IRLF 


B    3    flflT 


-V  f 


THE  LIBRARY 

OF 

THE  UNIVERSITY 
OF  CALIFORNIA 


PRESENTED  BY 

PROF.  CHARLES  A.  KOFOID  AND 
MRS.  PRUDENCE  W.  KOFOID 


An  Introduction 


to 


Vertebrate  Embryology 

Based  on  the  Study  of  the  Frog 
and  the  Chick 


By 
Albert  Moore  Reese,  Ph.D.  (Johns  Hopkins) 

Associate  Professor  of  Histology  in  Syracuse  University,  and  Lecturer  on 
Histology  and  Embryology  in  the  College  of  Medicine 


With  84  Illustrations 


G.  P.  Putnam's  Sons 
New  York  and  London 
Cbe  IRnfcfcerbocfeet:  press 

1904 


COPYRIGHT,  1904 

BY 
ALBERT  MOORE  REESE 

Published,  April,  1904 


Ube  ftnicfeerbocfeer  press,  Hew 


PREFACE 

THIS  small  volume  is  the  result  of  a  need 
that  the  author  has  felt,  for  some  years, 
for  a  concise  text-book  of  embryology 
that  described  the  development  of  both  the 
chick   and   the   frog.     The  only  other  single 
book,  with  which    the    author    is   acquainted, 
that  describes  the  development  of  both  these 
commonly  studied  forms  is  the  large  volume  of 
Marshall,  which  is  too  cumbersome  and  expen- 
sive for  a  general,  class  text-book. 

The  present  volume  is  intended  as  an  out- 
line, from  which  the  student  may  learn  the 
main  facts  about  the  embryology  of  the  two 
animals  in  question  ;  and  the  instructor  is  sup- 
posed in  his  lectures  to  enlarge  upon  this  out- 
line to  any  extent  that  he  may  see  fit.  Since 
the  needs  of  the  medical  student  have  been 
largely  considered  in  compiling  the  text,  very 
little  space  has  been  given  to  theoretical  dis- 
cussions ;  these  may  be  given  by  the  instructor, 
at  whatever  length  may  seem  desirable. 


vi  Preface 

For  purely  pedagogical  reasons,  the  develop- 
ment of  the  chick  has  been  described  by 
periods  ;  that  is,  all  the  changes  that  take  place 
during  a  certain  period  are  described  in  one 
section,  instead  of  describing  at  one  time,  the 
complete  development  of  any  one  organ. 

The  author  does  not  lay  claim  to  any  great 
originality  in  the  compilation  of  this  volume. 
He  has  sought  simply  to  collect,  into  conven- 
ient form,  the  more  important  facts  of  the  sub- 
ject under  discussion,  together  with  a  series  of 
figures  that  will  suitably  illustrate  these  facts. 

Marshall  and  Morgan  have  been  quoted  at 
length,  in  several  instances. 

Nearly  all  the  figures  ha\re  been  taken  from 
well-known  text-books  of  embryology,  the  au- 
thor being  stated  in  every  case. 

I  am  especially  indebted  to  Dr.  Charles  S. 
Minot  and  his  publishers,  P.  Blakiston's  Son 
&  Co.,  for  the  loan  of  the  electros  of  the  numer- 
ous figures  that  have  been  taken  from  Professor 
Minot's  recent  Laboratory  Text  of  Embryology 

ALBERT  M.   REESE. 

SYRACUSE  UNIVERSITY, 
March  /jr,  1904. 


CONTENTS 


CHAPTER  I 

PAGE 

THE    DEVELOPMENT    OF    THE    FROG  I 


CHAPTER  II 
THE    DEVELOPMENT    OF    THE    CHICK  -.  .  .         90 

CHAPTER  III 
THE    DEVELOPMENT    OF    THE    FIRST    DAY  .  .       I2O 

CHAPTER  IV 
THE    DEVELOPMENT    OF    THE    SECOND    DAY         .  .       139 

CHAPTER  V 
THE    DEVELOPMENT    OF    THE    THIRD    DAY  .  .       163 

CHAPTER  VI 

THE    DEVELOPMENT    OF    THE    FOURTH    DAY        .  .       222 

vii 


viii  Contents 

CHAPTER  VII 

PAGE 

THE    DEVELOPMENT    OF    THE    FIFTH    DAY  .  .       263 

CHAPTER  VIII 

THE   DEVELOPMENT    FROM    THE   SIXTH    DAY  TO    THE 

TIME    OF    HATCHING  .  .  .  .  .       279 

INDEX       . 285 


ILLUSTRATIONS 

THE  DEVELOPMENT  OF  THE  FROG 

FIGURE  PACK 

1.  Early  Stages  in  the  Development  of  the  Frog 

Embryo.     (From  a  photograph  of  Ziegler's 
wax  models)        .         .         .         Frontispiece 

2.  Egg  of  Starfish.     (After  Gegenbaur)       .         .         6 

3.  Ovarian  Egg  of  Frog       .....         7 

4.  Various    Stages   in   the    Development    of   the 

Frog.     (After  Brehm  from  Marshall)  .         8 

5.  Vertical  Sections  of  Segmenting  Eggs     .         .       19 

6.  Sections  of  Three  Stages  of  Segmentation  of 

the  Frog's  Egg  ......       20 

7.  Longitudinal  Vertical  Section  of  a  Frog  Em- 

bryo,  Showing  Commencing   Invagination. 
(After  Marshall) 22 

8.  Longitudinal  Vertical  Section  of  a  Frog  Em- 

bryo at  a  Later  Stage  in  the  Formation  of 

the  Mesenteron.      (After  Marshall)     .         .       23 

9.  Longitudinal  Vertical  Section  through  a  Frog 

Embryo,    Showing  the   Completion  of  the 
Mesenteron.     (After  Marshall)  ...       26 
10.   Transverse  Section  through  the  Middle  of  a 
Frog   Embryo,   at   about  the  Stage  Repre- 
sented in  Fig.  9.     (After  Marshall)     .         .       27 


x  Illustrations 

FIGURE  PAGE 

11.  Stages  in  the  Early  Development  of  the  Frog, 

Seen-  Obliquely  from  the  Posterior  End. 
(After  Ziegler  from  Marshall)  •.  .  .  30 

12.  A — Sagittal  Section  of  Embryo  Shown  in  Fig. 

n,  D.  B — Sagittal  Section  of  the  Embryo 
Shown  in  Fig.  nv  E  (After  Marshall)  .  33 

13.  Transverse  Section  of  a  Frog  Embryo  during 

the  Formation  of  the  Neural  Canal.  (After 
Marshall)  .  .  .  .*  .  .  -35 

14.  Sagittal  Section  of  a  Tadpole  at  the  Time  of 

Hatching.     (After  Marshall)  39 

15.  Transverse  Section  across  the  Middle  of  the 

Embryo  Shown  in  Fig.  n,  D.  (After  Mar- 
shall)   41 

16.  The  Brain  of  the  Frog.     (After  Marshall)        .       44 

17.  Longitudinal    Vertical    Section    through    the 

Anterior  End  of  a  Tadpole  Shortly  after 
Hatching.  (After  Marshall)  .  .  .  "  47 

1 8.  Longitudinal    Vertical    Section    through    the 

Anterior  Part  of  a  Tadpole  about  the  Time 
of  Appearance  of  the  Hind  Legs.  (After 
Marshall) 49 

19.  Half  Sections  in  the  Transverse  Plane  of  a 

Tadpole  10  mm.  Long  (left  half)  and  of  a 
Tadpole  12  mm.  Long  (right  half).  (After 
Marshall) 52 

20.  Transverse    Section   through  the   Head  of  a 

Tadpole  6%  mm.  in  Length,  about  the 
Time  of  Hatching.  (After  Marshall)  *  54 


Illustrations  xi 

FIGURE  PAGE 

21.  Transverse  Section  through  the  Region  of  the 

Hind-Brain  of  a  Young  Tadpole          .         .       57 

22.  Horizontal  Section  of  a  Tadpole  at  the  Time 

of  Hatching.     (After  Marshall)  ...       59 

23.  Diagrammatic    Figures   of  a  y-mm.   Tadpole, 

Shortly  after  Hatching,  Showing  the  Ar- 
rangement of  the  Blood  Vessels:  A — from 
Below;  B— from  the  Side.  (After  Marshall)  63 

24.  A  i2-mm.  Tadpole,  Dissected  from  the  Ventral 

Side.     (After  Marshall)       ....       65 

25.  Diagrams  to  Illustrate  the  Mode  of  Develop- 

ment of  the  Heart       .....       68 

26.  A  Diagrammatic  Figure  of  the  Head  and  Neck 

of  a  i2-mm.  Tadpole,  from  the  Right  Side, 
to  Show  the  Heart  and  Branchial  Vessels. 
Gills  and  Gill  Capillaries  not  Represented. 
(After  Marshall) 71 

27.  Diagrammatic  Figure  of  the  Arterial  System 

of  the  Male  Frog,  from  Right  Side.  (After 
Marshall)  .......  73 

28.  A  4o-mm.  Tadpole  Dissected  from  the  Ventral 

Surface.     (After  Marshall).          ...       76 

29.  A  Tailed  Frog,   near  the  Close  of  Metamor- 

phosis, Dissected  from  the  Ventral  Surface. 
(After  Marshall) 80 

30.  Diagrams  to  Illustrate  the  Development  of  the 

Head-Kidney.  (Somewhat  altered  from 
Morgan)  .......  82 


xii  Illustrations 

FIGURE  PAGE 

31.  Transverse    Section  through   the  Body   of   a 

Tadpole  at  the  Time  of  Hatching.  (After 
Marshall) 84 

32.  The  Skull  of  a  i2-mm.  Tadpole:  A — seen  from 

the  Right  Side;  B — seen  from  Dorsal  Side; 
C — seen  from  the  Ventral  Surface.  (After 
Marshall) 86 

THE  DEVELOPMENT  OF  THE  CHICK 

33.  Semi-Diagrammatic  View  of  the   Egg  of  the 

Fowl,  at  the  Time  6f  Laying.  (After  Parker 
and  Haswell,  slightly  altered  from  Mar- 
shall) .  . 92 

34.  A — Yolk  with  the  Blastoderm  in  the  Centre, 

the  Latter  Showing  the  First  Two  Cleavage 
Planes.  B — The  Blastoderm  on  a  Larger 
Scale  and  at  a  Later  Stage  of  Segmentation. 
(After  Duval) 96 

35.  Surface  View  of  the  Blastoderm   at  a  Later 

Stage  of  Segmentation  than  that  Shown  in 
Fig.  34,  B.  (After  Duval)  ...  98 

36.  Longitudinal  Section  of  the  Blastoderm  after 

the  Completion  of  Segmentation.  (After 
Duval) 104 

37.  Series  of  Diagrams  to  Illustrate  the  Formation 

of  the  Chick  Embryo,  Especially  the  Rela- 
tions of  the  Embryo,  Yolk- Sac,  Amnion, 
and  Allantois.  (After  Foster  and  Balfour), 

106,  109,  112 


Illustrations  xiii 

FIGURE  PAGE 

38.  A— B— C — D— Diagrams  Illustrating  the  De- 

velopment of  the  Foetal  Membranes  of  a 
Bird.     (After  Parker  and  Haswell)      .     117,118 

39.  Part  of  a  Section  through  the  Blastoderm  after 

the  Formation  of  the  Definite  Entoderm  or 
Hypoblast.  (After  Duval)  .  .  .121 

40.  Surface  View  of  the  Embryo  at  about  the  Six- 

teenth Hour  of  Incubation.     (After  Duval)     122 

41.  Median  Portion  of  a  Transverse  Section  of  an 

Embryo  at  the  Time  of  Formation  of  the 
Primitive  Streak.  (After  Duval)  .  .124 

42.  Transverse   Section   of  an   Embryo  of  about 

Twenty-one  Hours,  through  the  Anterior 
Part  of  the  Medullary  Folds.  (After  Duval)  126 

43.  Three  Transverse  Sections  across  the  Caudal 

End  of  the  Medullary  Groove  of  a  Chick 
Embryo  with  Seven  Segments.  (After 
Minot) 128 

44.  Surface  View  of  Embryo  at  the  Twenty-third 

Hour  of  Incubation.     (After  Duval)  .         .129 

44A.  Anterior  End  of  the  Preceding  Figure,  More 
Highly  Magnified  to  Show  the  Details. 
(After  Duval) 131 

45.  Sagittal  Section  of  an  Embryo  of  Twenty-six 

Hours.     (After  Duval)        ....     133 

46.  Diagrammatic  Representations  of  Chick  Em- 

bryos: A  —  after  Twenty  Hours'  Incuba- 
tion; B — after  Twenty-four  Hours'  Incuba- 
tion. (After  Parker  and  Haswell  from 
Marshall) 136 


xiv  Illustrations 


FIGURE 


47.  Surface  View  (dorsal)  of  an  Embryo  of  Thirty- 

three  Hours.     (After  Duval)       .         .         .     140 

48.  Transverse   Section  of  a  Chick  Embryo  with 

Seven  Segments,  to  Show  the  Beginning  of 

the  Formation  of  the  Heart.     (After  Minot)     142 

49.  Ventral  View  of  the  Anterior  Region  of  the 

Embryo  Shown  in  Fig.  47.     (After  Duval)       146 

50.  Sagittal  Section  of  the  Embryo  Shown  in  Fig. 

47.     (After  Duval)     .         .         .         .         .     150 
5oA.  Diagrammatic    Representation    of    Fig.    50. 

(After  Foster  and  Balfour)  .         .  152 

5 1 .  Sagittal  Section  of  an  Embryo  Chick  of  Eighty- 

two  Hours.     (After  Duval)          .         .         .      153 

52.  Transverse  Section  of  a  Chick  Embryo  with 

about  Twenty-eight  Segments.  (After  Minot)     156 

53.  Transverse  Section  through  the  Heart  Region 

of  an  Embryo  of  Thirty-three  Hours.  (After 
Duval) 158 

54.  Transverse  Section  through  the  Dorsal  Region 

of  an  Embryo  of  Forty-six  Hours.  (After 
Duval)  .......  159 

55.  Transverse  Section  through  a  Chick  Embryo 

to  Show  a  Slightly  Later  Stage  in  the  De- 
velopment of  the  Heart  than  is  Shown  in 
Fig.  48.  (After  Minot)  .  .  .  .161 

56.  Diagram  of  the  Circulation  of  a  Chick  Embryo 

at  the  End  of  the  Third  Day  of  Incubation, 

as  Seen  from  Below.     (After  Minot)  .         .     166 

57.  Surface  View  of  an  Embryo  of  Fifty-two  Hours. 

(After  Duval) 175 


Illustrations  xv 

FIGURE  PAGE 

58.  Transverse     Section     through     the    Anterior 

Region   of   a    Chick    Embryo    with    about 
Twenty-eight  Segments.     (After  Minot)     .     177 

59.  Transverse     Section     through     the    Anterior 

Region    of    a    Chick    Embryo   with    about 
Twenty-eight  Segments.     (After  Minot)      .     180 

60.  Transverse  Section  through  the  Fore-Brain  of 

a  Chick  of  Fifty  to  Sixty  Hours'  Incubation     182 

61.  The  Eye  of  a  Bird:  A — Sagittal  Section;  B — 

Surface  View  of  Entire  Organ.     (After  Par- 
ker and  Haswell  from  Vogt  and  Yung)        .     184 

62.  Transverse     Section     through     the    Anterior 

Region  of  a  Chick  Embryo  of  about  Twenty- 
eight  Segments.     (After  Minot)  .        ..         .     186 

63.  Transverse  Section  through  the  Anterior  Part 

of  an  Embryo  of  Sixty-eight  Hours.     (After 
Duval) 192 

64.  The  Head  of  an  Embryo  Chick  at  the  End  of 

the    Fifth   Day  of  Incubation,    Seen    from 
Below.     (After  Marshall)   .         .         .         .196 

65.  Diagram   of   the   Arterial  Circulation  on  the 

Third  Day.     (After  Foster  and  Balfour)     .     200 

66.  Diagram   of   the   Venous   Circulation   of  the 

Third  Day.     (After  Foster  and  Balfour)     .     201 

67.  Diagram  of  a  Portion  of  the  Digestive  Tract  of 

a  Chick  Embryo  during  the   Fourth   Day. 
(Foster  and  Balfour  from  Gotte)          .         .     205 

68.  Transverse    Section    of    an    Embryo    of   the 

Fourth  Day.     (After  Duval)       .         .         .208 


xvi  Illustrations 

FIGURE  PAGE 

69.  Transverse  Section  just  Posterior  to  the  Pre- 

ceding.    (After  Duval)       .         .         .         .213 

70.  Transverse  Section  through  the  Dorsal  Region 

of  an  Embryo  of  Sixty-eight  Hours.  (After 
Duval) 215 

71.  Transverse  Section  Anterior  to  the  Preceding. 

(After  Duval) 219 

72.  Two  Stages  in  the  Development  of  the  Chick 

Embryo:  A— at  about  the  Fifth  Day;  B — 
at  about  the  Ninth  Day.  (After  Parker 
and  Haswell  from  Duval)  .  .  .  .225 

73.  Transverse  Section  through  the  Dorsal  Region 

of  a  Chick  Embryo  of  Ninety-six  Hours. 
(After  Duval) 231 

74.  Transverse    Section     through     the     Wolffian 

Body.     (After  Duval)         .         .         .         .239 

75.  Heart  of  a  Chick  on  the  Fourth  Day,  Ventral 

View.     (After  Foster  and  Balfour)      .         .     242 

76.  Diagrammatic   Figure    Showing  the   Arrange- 

ment of  the  Blood  Vessels  in  a  Chick  Em- 
bryo at  the  End  of  the  Fifth  Day.  (After 
Marshall) 247 

77.  Diagram  of  the  Venous  Circulation  at  the  Com- 

mencement of  the  Fifth  Day.  (After  Foster 
and  Balfour) 252 

78.  Diagram  of  the  Venous  Circulation  during  the 

Later  Days  of  Incubation.     (After  Foster 

and  Balfour)        ....      ...   .      .     256 


Illustrations  xvii 

FIGURE  PAGE 

79.  Diagram  of  the  Venous  Circulation  after  the 

Commencement  of  Respiration  by  Means  of 

the  Lungs.     (After  Foster  and  Balfour)       .     257 

80.  Egg  of  Chick  with  Embryo  and  Foetal  Appen- 

dages. (After  Parker  and  Haswell  from 
Duval)  .......  266 

81.  Two  Views  of  the  Heart  of  a  Chick  on  the 

Fifth  Day  of  Incubation:  A— Ventral;  B — 
Dorsal  View.  (After  Foster  and  Balfour)  .  268 

82.  Heart  of  a  Chick  on  the  Sixth  Day,  Ventral 

View.     (After  Foster  and  Balfour)      .         .     269 

83.  Transverse  Section  through  the  Dorsal  Region 

of  a  Chick  Embryo  with  about  Twenty-eight 
Segments.  (After  Minot)  .  .  .  .271 

84.  Section   through  an  Advanced  Embryo   of  a 

Rabbit,  to  Show  how  the  Pericardial  Cavity 
Becomes  Surrounded  by  the  Pleural  Cavi- 
ties. (After  Foster  and  Balfour)  .  .  274 


AN  INTRODUCTION  TO 
VERTEBRATE  EMBRYOLOGY 

CHAPTER  I 

THE  DEVELOPMENT  OF  THE  FROG 
INTRODUCTION 

THE  eggs  of  the  common  frogs  (Rana  tern- 
poraria  and  allied  species)  may  usually 
be  found  without  difficulty  in  small 
ponds  and  pools  of  water,  where  they  are  laid,  in 
the  early  spring,  soon  after  the  melting  of  the 
ice.  They  may  easily  be  kept  alive,  in  the 
laboratory,  in  shallow  dishes  of  water,  and  their 
entire  development  thus  observed.  Their  rate 
of  development  varies  greatly  with  the  tem- 
perature, so  that  if  it  be  desirable,  for  any 
reason,  to  hurry  the  development,  all  that  is 
necessary  is  to  place  the  aquarium  in  a  warm 
place  ;  or  if  it  be  desired  to  keep  a  lot  of  eggs 


2  Vertebrate  Embryology 

in  a  certain  state  of  development,  this  may  be 
accomplished  by  keeping  the  aquarium  in  a  cool 
place  or  by  putting  lumps  of  ice  in  the  water. 

During  the  act  of  spawning,  which  may  last 
several  days,  the  male  clasps  the  female  firmly 
with  his  fore  legs  and  fertilizes  the  eggs  as 
they  leave  the  cloaca.  With  the  act  of  spawn- 
ing the  parental  instinct  ceases,  and  the  eggs 
are  left  to  themselves,  to  develop  or  perish  as 
the  case  may  be. 

As  in  the  laboratory,  so  in  nature,  the  rate 
of  development  depends  upon  the  temperature 
of  the  water,  but  in  a  few  days  or  a  week  the 
eggs  have  lost  their  spherical  form  and  have  be- 
come ovoid  in  shape;  and  in  about  ten  days  the 
head,  body,  and  tail  are  marked  off  from  each 
other  by  slight  constrictions.  The  embryo  now 
elongates  rapidly  and  by  the  end  of  the  second 
week  is  provided  with  three  pairs  of  tiny  ex- 
ternal gills,  and  is  able  to  work  its  way  out  of 
the  jelly-like  mass  with  which  it  is  surrounded, 
and  to  swim  freely  in  the  water.  At  this  time 
it  has  no  true  mouth,  and  so  is  dependent,  for 
growth,  upon  the  granules  of  yolk  which  were 
contained  in  the  egg.  For  several  days,  until 
the  appearance  of  the  mouth,  the  tadpole  is  pro- 
vided with  a  horseshoe-shaped  sucker  on  the 


The  Development  of  the  Frog        3 

lower  side  of  the  head,  by  means  of  which  it 
attaches  itself  to  any  solid  body  that  may  be  in 
the  water. 

As  the  mouth  is  being  formed,  the  digestive 
tract  becomes  greatly  elongated,  so  that  the 
abdominal  region  of  the  body  becomes  rounded 
and  swollen  by  the  coiled  mass  of  the  intestine 
lying  within.  Being  now  provided  with  horny 
jaws,  the  young  tadpole  feeds  actively  upon 
the  plants  of  its  habitat,  and  is,  therefore,  no 
longer  dependent  upon  the  yolk  for  growth. 

The  gill-clefts  make  their  appearance,  at 
about  this  time,  as  four  pairs  of  slit-like  open- 
ings which  connect  the  pharynx  with  the  ex- 
terior. The  edges  of  these  slits  become  folded 
to  form  the  internal  gills,  and  as  the  internal 
gills  increase  in  size,  the  external  gills  gradu- 
ally diminish  and  are  covered  by  two  folds 
of  skin  which  grow  back  over  them  from  in 
front.  These  two  opercular  folds  fuse  to- 
gether along  the  mid-ventral  line,  and  their 
posterior  edges  fuse  with  the  body-wall  behind 
the  gills,  so  that  the  latter  are  completely  en- 
closed except  for  a  sort  of  spout  on  the  left 
side,  through  which  water,  taken  into  the  gill- 
chamber  through  the  mouth,  to  bathe  the  gills, 
passes  again  to  the  exterior. 


4  Vertebrate  Embryology     , 

The  young  tadpole  has  now  practically  the 
structure  and  habits  of  a  fish,  but  very  soon 
the  rudiments  of  the  hind  legs  appear  as  small 
protuberances  at  the  base  of  the  tail,  one  on 
each  side  of  the  cloaca  ;  and  by  the  eighth  week 
the  joints  and  toes  are  formed,  and  the  legs 
have  about  the  same  structure  as  in  the  adult. 

The  fore  legs  are  formed  at  about  the  same 
time  as  are  the  hind  legs,  but  they  are  hidden, 
for  some  time,  by  the  operculurri.  The  left 
fore  leg,  in  the  course  of  two  or  three  weeks, 
projects  through  the  above-mentioned  opercu- 
lar  spout,  while  the  leg  of  the  opposite  side 
has  to  force  its  way  directly  through  the  oper- 
cular  fold. 

The  lungs,  in  the  meantime,  have  become 
functional  and  the  tadpole  frequently  comes  to 
the  surface  to  breathe,  although,  for  a  time, 
respiration  takes  place  by  means  of  both  lungs 
and  gills. 

Before  this  remarkable  metamorphosis  is 
complete  and  the  frog  is  ready  to  begin  life  as 
an  air-breathing  animal,  the  tail  must  be  com- 
pletely absorbed,  the  mouth,  eyes,  and  other 
structures  must  be  greatly  changed,  and  the 
gills,  gill-clefts,  and  other  fish-like  structures 
must  diminish  or  entirely  disappear. 


The  Development  of  the  Frog        5 
THE  EGG 

Since  every  animal  begins  its  individual  ex- 
istence as  an  ovum  or  egg,  it  may  be  well, 
before  taking  up  the  study  of  the  frog's  egg, 
to  examine  some  egg  that  will  more  easily  show 
the  different  structures  of  a  typical  ovum,  the 
frog's  egg  being  so  large  and  so  full  of  yolk 
that  it  is  difficult  for  the  beginner  to  distin- 
guish its  different  parts.  For  this  purpose  the 
eggs  of  the  starfish,  or  of  the  sea-urchin,  are 
very  convenient,  and  if  some  of  these  eggs  be 
properly  stained  and  mounted,  the  main  fea- 
tures of  their  structure  may  be  made  out  with- 
out difficulty. 

The  ovum,  whether  it  be  of  microscopic 
size  or  30  mm.  in  diameter,  as  is  the  yolk  of 
the  hen's  egg,  is  always  a  single  cell.  Al- 
though the  egg  of  the  common  starfish  is  only 
as  large  as  a  small  grain  of  sand,  yet  if  it 
be  examined  under  a  moderate  magnification 
of  the  microscope,  it  will  be  found  to  be  made 
up  of  several  distinct  parts.  Like  most  ova 
it  is  spherical  in  shape,  and  is  enclosed  in  a 
thin  cell-wall  or  vitelline  membrane  (Fig.  2). 
In  the  granular,  protoplasmic  contents  of  the 
egg  two  regions  may  be  distinguished :  a 


6  Vertebrate  Embryology 

lighter  portion  which  makes  up  the  greater 
part  of  the  egg  and  which  is  known  as  the 
cytoplasm,  and  a  darker,  spherical  portion  which 
lies  in  the  cytoplasm  and  is  known  as  the 
nucleus  (germinal  vesicle).  Inside  of  the  nu- 
cleus may  be  seen  one  or  more  small  areas, 
the  nucleoli  (germinal  spots) 


FIG.  2.— EGG  OF  STARFISH.    (After  Gegcnbaur.) 

a.  Granular  protoplasm. 

b.  Nucleus  (germinal  vesicle). 

c.  Nucleolus  (germinal  spot). 


By  the  use  of  more  refined  methods  and 
higher  magnification  many  other  details  of 
structure  might  be  brought  out,  but  for  these 
the  reader  is  referred  to  more  extensive  text- 
books. 

The  frog's  egg  is  several  thousand  times  the 
bulk  of  the  egg  of  the  starfish,  being  about 
1.7  mm.  in  diameter.  This  increase  in  size  is 


The  Development  of  the  Frog        7 

chiefly  due  to  the  large  amount  of  food-yolk 
contained  in  the  frog's  egg  (Fig.  3.) 

As  the  eggs  ripen  and  are  set  free  from  the 
ovary,  they  fall  into  the  body  cavity  and  pass 
forward  into  the  abdominal  openings  of  the 
oviducts.  Passing  slowly  along  these  ducts, 
the  eggs  at  last  collect  in  large  numbers  in  the 


FIG.  3. — OVARIAN  EGG  OF  FROG. 

thin-walled,  dilated  posterior  parts  of  the  ovi- 
ducts, where  they  remain  until  they  are  forced 
out  into  the  water  at  the  time  of  spawning. 

Owing  to  the  opacity  of  the  frog's  egg,  the 
nucleus  is  only  visible  in  sections,  although  it 
is  very  large,  sometimes  as  much  as  one-third 
to  one-half  the  diameter  of  the  egg  (Fig.  3). 

Before  it  is  set  free  from  the  ovary,  the  egg 
has  secreted  around  it,  in  some  way  that  is  not 
well  understood,  a  thin  vitelline  membrane ; 


8 


Vertebrate  Embryology 


and  as  it  passes  through  the  anterior,  thick- 
walled  part  of  the  oviduct  a  gelatinous  envel- 
ope is  deposited  around  it.  This  envelope,  on 
coming  in  contact  with  the  water,  swells  enor- 
mously, and  forms  a  mass  of  colorless  jelly, 
characteristic  of  frog's  spawn  (Fig.  4).  The 


FIG.  4.— VARIOUS  STAGES  IN  THE  DEVELOPMENT  OF  THE  FROG. 
(After  Brehm    from  Marshall.) 

1.  Eggs  just  laid.  2.  Eggs  shortly  after  laying.  3.  Tadpole  shortly  before 
hatching.  4.  Tadpoles  just  hatched.  5  and  6.  Tadpoles  with  external  gills. 
7  and  8.  Tadpoles  with  fully-formed  opercular  folds.  9  and  10.  Tadpoles  with 
well-developed  hind  legs,  shortly  before  the  metamorphosis.  11.  Tadpole  during 
the  metamorphosis.  12.  Young  frog  with  tail  only  partially  absorbed. 


thin,  gelatinous  envelope  is  said  to  begin  to 
swell  about  one  minute  after  it  comes  in  con- 
tact with  the  water,  and  to  reach  its  greatest 
expansion  in  three  hours.  Its  purpose  is  to 
protect  the  soft  eggs  from  being  injured  by 


The  Development  of  the  Frog       9 

contact  with  surrounding  objects,  and  also  to 
hasten  development  by  storing  up  heat,  this 
latter  power  being  due  to  the  fact  that  it  per- 
mits the  heat  of  the  sun  to  pass  inward  more 
rapidly  than  it  permits  the  reflected  heat  to 
pass  out  again,  with  the  result  that  the  mass 
of  spawn,  in  the  sunlight,  is  warmer  than 
the  surrounding  water.  The  jelly  may  also 
protect  the  eggs  from  being  eaten  by  other 
animals. 

The  egg  itself  consists  of  a  black  and  a  white 
pole  of  approximately  equal  sizes,  the  dark 
color  of  the  black  hemisphere  being  due  to 
the  presence  of  a  superficial  layer  of  pigment 
in  that  region.  The  origin  of  this  pigment  is 
not  clearly  understood,  but  its  purpose  seems 
to  be  that  of  absorbing  the  heat  of  the  sun, 
and  in  furtherance  of  this  object  the  pigmented 
half  of  the  egg  is  of  less  specific  gravity  than 
the  other  half,  with  the  result  that  the  dark 
pole  is  always  the  upper  one  and  the  one  in 
which  the  segmentation  takes  place  the  more 
rapidly.  This  automatic  orientation  is  made 
possible  by  the  fact  that  the  egg  shrinks  away 
from  its  vitelline  membrane,  between  which 
and  itself  is  secreted  a  small  quantity  of  fluid 
in  which  the  egg  may  easily  rotate. 


io  Vertebrate  Embryology 

A  mass  of  frog's  spawn  may  be  compared 
to  a  number  of  hen's  eggs  which  have  been 
carefully  broken  into  a  dish,  so  that  the  yolks 
are  all  unbroken.  The  yolks  of  the  hen's  eggs 
correspond  to  the  true  eggs  of  the  frog's  spawn, 
and  the  white  of  the  hen's  egg  to  the  jelly 
mass  of  the  spawn.  The  white  of  the  hen's 
egg,  however,  serves  as  food  for  the  develop- 
ing chick,  while  the  jelly  of  the  spawn  probably 
serves  no  such  purpose. 

Maturation  of  the  Egg 

As  a  rule,  before  an  egg  may  begin  its  de- 
velopment, it  must  be  fertilized,  and  before  it 
can  be  fertilized  it  must  undergo  a  process  of 
ripening  or  maturation.  The  details  of  this 
maturation  vary  in  different  eggs,  but  the  es- 
sential processes  are  about  the  same  in  all. 

As  has  been  stated  above,  the  egg  of  the 
frog,  when  just  set  free  from  the  ovary,  con- 
tains a  very  large  nucleus.  It  is  the  nucleus 
that  is  chiefly  concerned  in  the  maturation 
changes,  and  the  first  change  that  is  noticed  is 
a  shrinkage  of  this  large  nucleus  and  a  loss  of 
the  nuclear  membrane.  After  passing  through 
other  changes,  a  description  of  which  cannot 
be  given  here,  the  nucleus  divides  into  two 


The  Development  of  the  Frog       1 1 

equal  parts,  and  one  of  these  halves  is  extruaed 
from  the  egg  and  lies  under  the  vitelline  mem- 
brane at  the  upper  or  black  pole.  This  ex- 
truded half  of  the  nucleus  is  known  as  theyfrj/ 
polar  body,  and  its  formation  takes  place  while 
the  egg  is  still  in  the  oviduct  of  the  frog. 
Shortly  after  the  egg  is  laid  and  the  sperm  has 
entered  it,  the  half  of  the  nucleus  that  remained 
after  the  formation  of  the  first  polar  body  again 
divides  into  equal  parts,  and  the  second  polar 
body  is  extruded.  The  part  of  the  nucleus  that 
remains  after  the  formation  of  the  polar  bodies 
is  known  as  the  female  pronucleus,  and  con- 
tains, as  may  easily  be  understood,  just  one- 
fourth  of  the  material  of  the  original  egg 
nucleus.  The  two  small  round  polar  bodies, 
lying  side  by  side  under  the  vitelline  membrane 
at  the  dark  pole  of  the  egg,  take  no  further 
part  in  the  development  of  the  egg,  and  eventu- 
ally disappear. 

What  the  purpose  of  the  maturation  of  the 
egg-cell  may  be  it  is  not  possible  at  the  present 
time  to  say  ;  and  so  many  theories  on  the  sub- 
ject have  been  advanced  that  it  is  very  difficult 
to  give  any  simple  statement  of  the  case. 

The  formation  of  the  polar  bodies  or  glob- 
ules is  the  result  of  a  form  of  cell  division 


12  Vertebrate  Embryology 

known  as  "  reduction  division."  When  the 
first  globule  is  formed,  it  is  by  the  division  of 
the  egg-cell  into  two  cells,  a  large  one  and  a 
very  small  one,  the  small  one  being  the  polar 
globule.  In  like  manner  the  second  globule 
is  formed  by  the  very  unequal  division  of  the 
larger  of  the  first  two  cells,  the  larger  cell  of 
the  latter  division  being  the  true  female  element 
which  is  capable  of  being  fertilized. 

The  essential  element  of  the  nucleus,  that 
part  which  is  especially  concerned  in  heredity, 
or  the  transmission  of  parental  characteristics, 
seems  to  be  the  chromosome.  The  number  of 
chromosomes  in  the  nucleus  of  any  given 
species  is  normally  constant. 

It  has  been  found  that  the  number  of 
chromosomes  in  the  egg  after  maturation  is 
just  half  what  it  was  before  that  process,  and 
the  amount  of  chromatin  is  reduced  to  one 
quarter  of  the  original  quantity. 

O.  Hertwig  thinks  that  the  reduction  divi- 
sions taking  place  in  maturation  are  for  the 
purpose  of  increasing  the  relative  amount  of 
cytoplasm,  rather  than  for  reducing  the  quan- 
tity of  nuclear  material.  The  cell  that  is  left 
after  the  extrusion  of  the  polar  bodies,  although 
containing  only  one  fourth  of  the  original 


The  Development  of  the  Frog      13 

chromatin,  has  retained  practically  all  of  the 
cytoplasm  ;  so  that  the  result  of  the  formation 
of  the  polar  bodies  is  practically  to  increase  the 
cytoplasm  fourfold.  The  objections  to  this 
theory  cannot  be  given  here. 

One  of  the  oldest  and  most  celebrated  the- 
ories in  regard  to  the  formation  of  the  polar 
bodies  is  that  of  Minot.  According  to  this 
theory  the  fertilized  egg-cell  is  said  to  be 
hermaphrodite,  that  is,  it  is  both  male  and 
female,  since  it  is  formed  by  the  fusion  of  the 
male  and  female  elements.  When  the  fertilized 
egg  divides  for  the  first  time  the  nuclear  ma- 
terial is  equally  divided  between  the  two  blas- 
tomeres  that  are  formed,  so  that  each  of  these 
blastomeres  must  be  hermaphrodite.  If  this 
be  true  of  the  first  two  blastomeres,  it  must  be 
equally  true  of  all  the  cells  that  are  formed  by 
the  repeated  division  of  the  original  egg-cell  : 
hence  the  unfertilized  egg-cell  developed  from 
the  original  egg  must  also  be  hermaphrodite ; 
and  before  it  can  receive  additional  male  chro- 
matin, in  the  act  of  fertilization,  it  must  get  rid 
of  the  male  chromatin  that  it  already  possesses, 
by  extruding  the  polar  bodies. 

If  this  theory  were  true,  it  is  evident  that  a 
child  could  not  inherit  the  characters  of  its 


14  Vertebrate  Embryology 

mother's  father,  nor  the  characters  of  any  of 
its  father's  ancestors. 

Delage  and  Herouard  have  elaborated  a 
theory  that  is,  briefly,  as  follows  :  The  simplest 
organisms  are  capable  of  reproducing  them- 
selves indefinitely  by  a  process  of  repeated 
division.  More  highly  organized  beings  are 
not  possessed  of  this  indefinite  power  of  di- 
vision, and  must  occasionally  undergo  a  process 
of  fusion  or  conjugation.  This  process  con- 
sists of  two  parts,  the  elimination  of  chromatic 
material  (maturation),  and  the  conjugation 
proper,  or  fertilization.  The  maturation  is  usu- 
ally considered  as  an  accessory  phenomenon, 
whose  object  is  simply  to  make  the  fertiliza- 
tion possible,  but,  according  to  this  hypothesis, 
"  The  essential  phenomenon  is  the  chromatic 
reduction,  and  the  fecundation  is  an  addition 
which  is  advantageous  but  not  indispensable." 

In  the  simplest  organisms  metabolism  is  a 
closed  cycle  ;  but  in  more  complicated  beings 
this  is  not  the  case,  and  there  is  gradually 
accumulated  a  substance  which  is  injurious 
and  which  affects  all  the  functions  of  life, 
especially  those  concerned  in  cell  division. 
Unless  this  substance  is  gotten  rid  of,  the  cell 
will  die. 


The  Development  of  the  Frog       15 

In  the  case  of  the  tissue  cells  of  the  higher 
organisms  there  is  no  method  of  removing  this 
substance,  so  that  these  cells  must  eventually 
perish  ;  but  in  the  case  of  the  simplest  uni- 
cellular organisms,  and  in  the  reproductive 
cells  of  the  higher  forms,  this  substance  is 
removed  in  a  single  operation,  and  the  cell 
thus  enabled  to  begin  a  new  series  of  di- 
visions. 

Labbe  found  among  certain  insects  a  reduc- 
tion of  chromatin,  not  followed  by  fecundation, 
that  was  followed  by  cell  division  and  develop- 
ment ;  and  other  cases  of  parthenogenesis  are 
known. 

The  expulsion  of  chromatic  material  is  rep- 
resented in  higher  organisms  by  the  extrusion 
of  the  first  polar  body,  and  "  if  one  could 
prevent  the  extrusion  of  the  second  polar 
body,  all  beings  would  develop  parthenogen- 
etically." 

The  formation  of  the  second  polar  body 
reduces  the  amount  of  chromatin  and  the  num- 
ber of  chromosomes,  and  makes  impossible 
further  development,  until  fresh  chromatic 
material  has  been  added  by  the  process  of 
fecundation. 

It  will   be  seen   from  the  above  examples 


1 6  Vertebrate  Embryology 

that  the  processes  of  maturation  and  fertiliza- 
tion offer  a  wide  field  for  speculation,  but  one 
into  which  it  is  not  within  the  province  of  this 
book  to  enter. 

Fertilization  of  the  Egg 

As  the  eggs  are  extruded  from  the  cloaca  of 
the  female,  which  process  may  take  place  in  a 
few  minutes  or  may  be  prolonged  over  several 
days,  the  spermatozoa  are  spread  over  them 
by  the  male  and  at  once  begin  to  bore  their 
way  through  the  jelly  towards  the  eggs. 

The  exact  nature  of  the  changes  that  take 
place  after  the  sperm  enters  the  egg  has  not 
been  entirely  determined,  but  the  essential 
points  will  be  given.  A  few  minutes  after 
coming  in  contact  with  the  vitelline  membrane, 
the  head  of  the  spermatozoon  works  its  way 
into  the  egg  and  moves  towards  the  female 
pronucleus,  with  which  it  fuses  to  form  the 
so-called  segmentation  nucleus.  The  head  of 
the  spermatozoon,  after  it  has  entered  the 
egg,  is  known  as  the  male  pronucleus,  and  the 
essential  act  of  fertilization  is  the  fusion  of 
the  male  and  female  pronuclei.  The  tail  of 
the  spermatozoon  remains  outside  of  the  egg 
and  apparently  takes  no  part  in  the  process 


The  Development  of  the  Frog       1 7 

of  fertilization  ;  the  fate  of  the  middle-piece, 
in  the  frog,  is  not  well  understood,  but  it  is 
possible  that  it  may  effect  segmentation  in 
some  way.  As  a  rule,  only  one  spermatozoon 
enters  the  egg,  but  it  is  likely  that  if  two  or 
more  spermatozoa  reach  the  vitelline  mem- 
brane at  the  same  time,  they  may  all  enter  the 
egg,  although  only  one  male  pronucleus  will 
fuse  with  the  female  pronucleus.  In  some 
other  animals  the  entrance  of  two  or  more 
spermatozoa  into  the  egg  (polyspermy)  pro- 
duces serious  results,  causing  irregularities  in 
segmentation  ;  but  in  the  frog  the  extra  pro- 
nuclei  probably  disappear  without  producing 
any  unusual  effect. 

Segmentation  of  the  Egg 

About  two  or  three  hours  (depending  on 
the  temperature)  after  fertilization,  the  first  in- 
dication of  segmentation  is  seen  as  furrow  on 
the  dark  pole  of  the  egg.  This  furrow  gradu- 
ally extends  around  towards  the  white  pole 
until  it  completely  encircles  the  egg  (Fig.  i, 
B).  By  the  time  this  has  taken  place,  the 
contents  of  the  egg  have  been  separated  into 
two  parts  by  a  plane  corresponding  to  the 
superficial  furrow,  so  that  the  egg  is  now 


1 8  Vertebrate  Embryology 

completely  separated  into  two  blastomeres  of 
approximately  equal  size,  which,  at  first,  tend 
to  become  spherical  in  shape,  but  which  are 
soon  flattened  against  each  other  to  form 
hemispheres.  Before  the  formation  of  this 
first  cleavage  plane,  the  segmentation  nucleus 
has  divided  into  two  equal  parts,  one  of  which 
is  found  in  each  of  the  two  blastomeres.  In 
dividing,  the  nucleus  passes  through  a  com- 
plicated series  of  changes  known  as  karyoki- 
nesis,  for  a  description  of  which  the  reader  is 
referred  to  more  extensive  text-books.  The 
first  cleavage  plane  corresponds  to  the  medio- 
longitudinal  (sagittal)  plane  of  the  future  frog  : 
this,  however,  is  not  true  of  all  animals. 

After  a  short  resting  period,  the  second 
cleavage  plane  is  formed,  preceded,  as  in  the 
former  and  as  in  all  subsequent  cases,  by  the 
division  of  the  nucleus  of  each  blastomere. 
The  second  plane  is  also  a  vertical  one  begin- 
ning in  the  dark  pole,  and  is  at  right  angles  to 
the  first  plane.  The  egg  now  consists  of  four 
more  or  less  equal  blastomeres  (Fig.  i,  C). 

The  third  plane  is  normally  a  horizontal 
one,  at  right  angles  to  the  first  two,  but  not  in 
the  equatorial  plane  of  the  egg,  so  that  the  egg 
is  divided  into  eight  cells  (Fig.  i,  /?),  four 


The  Development  of  the  Frog      19 

small  dark  cells  at  the  upper  pole,  and  four 
larger  white  cells  at  the  lower  pole  ;  that  is  to 
say,  the  third  plane  is  horizontal  but  nearer  the 
upper  than  the  lower  pole  (Fig-.  5,  B). 

The  next  division  is  by  two  vertical  planes, 
at  right  angles  to  each  other  and  half-way 
between  the  first  two  planes.  Thus  we  have 


FIG.  5. — VERTICAL  SECTIONS  OF  SEGMENTING  EGGS. 

A,  2-cell  stage.    £,  8-cell  stage. 

the  egg  made  up  of  sixteen  blastomeres  (Fig. 
i,E). 

The  thirty-two-cell  stage  is  formed  by  two 
horizontal  planes,  one  above  and  one  below 
the  first  horizontal  plane  (Fig.  i,  F). 

After  the  thirty-two-cell  stage  the  segmenta- 
tion proceeds  so  rapidly  and  so  irregularly  that 
it  cannot  be  followed  with  certainty, — indeed 
it  is  seldom  that  the  processes  above  described 


20  Vertebrate  Embryology 

can  be  followed  as  far  as  the  thirty-two-cell 
stage,  irregularities  often  being  seen  as  early 
as  the  four-cell  stage. 

As  early  as  the  eight-cell  stage,  sections  of 


A  and  S,  early  and  late  stages  in  the  segmentation  of  the  egg.  C, 
beginning  of  the  archenteron,  Ar.  (gastrulation).  S  C,  segmentation- 
cavity  (camera  lucida  ;  C  slightly  altered). 

the  egg  (Fig.  5,  IT)  show  a  small  central  cavity, 
the  segmentation  cavity,  which  becomes  larger 
as  segmentation  proceeds,  and  is  filled  with  an 
albuminous  fluid.  This  cavity,  as  will  be  seen, 


The  Development  of  the  Frog      2 1 

eventually  disappears  and  forms  no  part  of  the 
adult  structure. 

After  the  thirty-two-cell  stage,  a  series  of 
concentric  segmentation  planes  are  formed, 
dividing  the  blastomeres  into  several  layers  of 
cells.  By  the  continuation  of  this  process  of 
cell-division  the  egg  is  eventually  divided  into 
several  hundred  cells  (Figs,  i,  6),  those  of 
the  dark  pole  being  much  smaller,  more  sharply 
defined,  and  more  numerous  than  those  of  the 
light  pole.  As  is  seen  in  the  figures,  the  seg- 
mentation cavity  lies  nearer  the  dark  pole,  so 
that  its  roof  is  composed  of  a  few  layers  of 
small,  dark  cells,  while  its  floor  is  made  up 
of  many  layers  of  ill-defined,  yolk-filled  cells. 
There  is,  however,  no  sharp  dividing  line  be- 
tween the  pigmented  and  unpigmented  cells, 
any  more  than  there  was  between  the  dark 
and  light  poles  of  the  unsegmented  egg. 

Formation  of  the  Germ-Layers 

The  egg,  at  the  close  of  segmentation,  has 
been  converted  into  a  hollow  sphere,  with  the 
cavity  nearer  the  upper,  or  dark  pole  (Fig.  6). 
The  cells  of  the  dark  hemisphere  are  arranged 
in  two  more  or  less  distinct  layers,  while  the 
large,  unpigmented  cells  have  no  such  regular 


22  Vertebrate  Embryology 

arrangement.  At  this  time  a  crescentic  groove 
appears  on  one  side  of  the  egg  at  the  bor- 
der between  the  white  and  dark  cells.  This 
groove,  whose  convex  side  is  upward,  is  the 
dorsal  lip  of  the  blastopore,  and  is  the  begin- 


EN 

FIG.  7. — LONGITUDINAL  VERTICAL  SECTION  OF  A  FROG 
EMBRYO,  SHOWING  COMMENCING  INVAGINATION.  X28. 
(After  Marshall). 

B,  blastopore.  EE,  outer  or  epidermic  layer  of  ectoblast.  EN, 
inner  or  nervous  layer  of  ectoblast.  S  C,  segmentation  cavity.  F, 
yolk-cells. 

ning  of  the  process  of  invagination  (Figs.  6, 
7,  and  8). 

The  horns  of  the  crescent  extend  towards 
each  other  until  they  meet  to  form  a  circle 
(Fig.  i,  //),  the  blastopore,  bounded  on  the 
outside  by  pigmented  cells,  and  filled  inside 


The  Development  of  the  Frog       23 

with  white  cells.  The  mass  of  white  cells 
which  fills  the  blastopore  is  known  as  the 
yolk-plug  (Y\g.  8,  YP\ 

By  a  rapid  division  of  the  black  cells  around 


YP — 


FIG.  8. — LONGITUDINAL  VERTICAL  SECTION  THROUGH 
A  FROG  EMBRYO  AT  A  LATER  STAGE  IN  THE  FORMATION 
OF  THE  MESENTERON.  (After  Marshall,) 

H^  invaginate  entoblast.  M,  mesoblast.  MN,  mesenteron. 
JV,  notochord.  SC,  segmentation  cavity.  KP,  yolk-plug,  filling  up 
the  blastopore. 

the  rim  of  the  blastopore,  especially  at  the  dor- 
sal lip,  the  exact  nature  of  which  process  is  in 
some  dispute,  the  diameter  of  the  blastopore  is 
gradually  reduced  and  the  yolk-plug  is  with- 
drawn into  the  egg  (Figs.  8  and  9). 

This  overgrowth  of  the  black  cells  continues 


24  Vertebrate  Embryology 

until  the  yolk-plug  entirely  disappears  from 
the  surface,  and  the  blastopore  is  reduced  to  a 
narrow  slit.  The  layer  of  black  cells,  which 
now  completely  surround  the  egg  or  embryo, 
is  the  upper  germ-layer  or  ectoblast  (Fig.  9). 

Carefully  prepared  sections  through  the 
embryo  at  the  time  of  the  appearance  of  the 
dorsal  lip  of  the  blastopore  may  show,  in 
the  region  where  the  white  and  black  cells 
meet,  a  more  or  less  clearly  defined  zone  of 
cells  extending  equatorially  around  the  em- 
bryo. This  band  is  several  cells  deep,  the 
inner  cells  passing  insensibly  into  the  yolk- 
cells,  the  peripheral  cells  being  indistinguish- 
able from  the  ectoblast. 

"  This  ring  of  cells,  as  subsequent  develop- 
ment shows,  is  the  beginning  of  the  embryo, 
and  the  ring  itself  is  composed  of  the  material 
which  subsequently  forms  the  central  nervous 
system,  the  mesoderm,  the  notochord,  and  a 
part  of  the  entoderm."  J 

By  a  process  of  concrescence,  which  is  closely 
related  to  the  closure  of  the  blastopore,  de- 
scribed above,  this  band  of  cells  shifts  towards 
one  side  of  the  embryo,  and  its  right  and  left 
halves  fuse  to  form  a  broad  meridional  band 

1  Morgan. 


The  Development  of  the  Frog      25 

extending  into  the  dorsal  lip  of  the  blastopore. 
This  process  may  be  roughly  illustrated,  per- 
haps, by  placing  a  rubber  band  around  the 
equator  of  a  ball,  and  then  gradually  slipping 
two  opposite  sides  of  the  band  towards  one 
pole  of  the  ball,  until  they  meet  and  form  a 
single  broad  band  lying  in  a  meridional  instead 
of  in  an  equatorial  position. 

This  process  of  concrescence  is  difficult 
of  determination,  and  it  will  probably  not  be 
practicable  for  students  to  work  it  out  in  the 
laboratory. 

As  has  been  said,  the  growth  of  the  ectoblast 
over  the  yolk-cells  takes  place  much  more 
rapidly  from  the  dorsal  lip  of  the  circular 
groove,  which  we  have  called  the  blastopore, 
so  that,  while  this  groove  never  becomes  very 
deep  on  the  lower  side,  on  the  upper  side  it 
becomes  a  long,  narrow  slit  extending  nearly 
to  the  opposite  side  of  the  embryo  (Fig.  9, 
MN}.  This  slit,  whatever  may  be  the  exact 
method  of  its  formation,  is  the  primitive  di- 
gestive tract  of  the  frog,  and  is  known  as  the 
mesenteron  or  archenteron.  It  is  much  wider 
from  side  to  side  than  it  is  in  a  dorso-ventral 
direction  ;  and  while  its  roof  is  made  up  of  a 
more  or  less  clearly  defined  layer  of  closely 


26  Vertebrate  Embryology 

packed  cells,   its   floor  is   a   mass  of  undiffer- 
entiated   yolk-cells.       The    cells   forming   the 
roof  of  the  mesenteron  are  the  beginning  of 
the  lower  germ-layer,  or  entoblast  (Fig.  9). 
The  mesenteron,  opening  to  the  exterior  by 


FIG.  9. — LONGITUDINAL  VERTICAL  SECTION  THROUGH 
A  FROG  EMBRYO,  SHOWING  THE  COMPLETION  OF  THE 
MESENTERON.  (After  Marshall.) 

B,  blastopore.  E  E,  epidermic  layer  of  ectoblast.  E  N,  nervous 
layer  of  ectoblast.  ff,  invaginate  entoblast.  J/,  mesoblast.  M  N^ 
mesenteron.  TV,  notochord. 

the  narrow  blastopore  (at  the  posterior  end 
of  the  embryo),  rapidly  enlarges  by  forward 
growth  and  by  the  depression  of  the  yolk-cells 
forming  its  floor,  until  it  becomes  a  large 
cavity  whose  growth  has  caused  the  oblitera- 
tion of  the  segmentation  cavity  (Figs.  8,  9,  and 


The  Development  of  the  Frog      27 

10).     The  mouth   and   true  anus  will  not  be 
formed  until  later. 

The    notochord,    or    primitive   backbone,    is 
formed  at  this  time  as  a  rod-like  thickening  of 


CH 

MM 


FlG.    10. — A  TRANSVERSE  SECTION  THROUGH  THE  MID- 
DLE OF  THE  LENGTH  OF  A  FROG  EMBRYO,  AT  ABOUT  THE 

STAGE  REPRESENTED  IN  FIG.  9.     (After  Marshall.) 

C//,  notochord.  .£",  ectoblast.  H ' M,  pouch-like  diverticulum 
of  the  entoblast  into  the  mesoblast.  M,  mesoblast.  N  G^  neural 
groove.  N P,  neural  plate.  7",  mesenteron.  }',  yolk. 

the  entoblast,  extending  along  the  roof  of  the 
mesenteron  in  the  middle  line  for  the  greater 
part  of  its  length.  It  does  not,  for  a  time,  sepa- 
rate from  the  rest  of  the  entoblast  and  is  very 
indistinct :  but  it  later  forms  a  distinct  rod  of 


28  Vertebrate  Embryology 

cells,  which  is  a  characteristic  feature  of  all 
transverse  sections  of  embryos  (Figs.  10,  12, 
13,  and  15). 

According  to  some  workers  the  notochord 
is  formed  by  a  condensation  and  differentiation 
of  mesoblast  cells  along  the  mid-dorsal  region 
of  the  embryo.  Since  the  mesoblast  and  ento- 
blast  are,  in  their  origin,  so  closely  associated, 
the  exact  method  of  formation  of  the  noto- 
chord, whether  from  the  one  layer  or  the  other, 
is  not  a  matter  of  very  great  importance  ;  but 
the  majority  of  workers  probably  support  the 
former  view, — that  is,  that  it  is  formed  by  a  dif- 
ferentiation of  a  part  of  the  entoblastic  layer. 

Like  the  formation  of  the  archenteron,  the 
origin  of  the  middle  germ-layer,  or  mesoblast, 
has  been  so  variously  described  by  different 
authors  that  it  is  quite  a  difficult  matter  to 
decide  which  is  the  most  probable  view.  Al- 
though so  difficult  of  determination  in  the 
case  of  the  frog,  the  origin  of  the  mesoblast 
in  some  other  animals  is  easily  made  out. 

Marshall  states  that  it  "arises  in  the  frog  as 
two  lateral  sheets  of  cells,  split  off  from  the 
outer  surface  of  the  hypoblast  and  yolk-cells." 

Morgan  says  "  .  .  .  the  cells  that  are  to  form 
the  mesodermal  layer  are  present  at  the  time  when  the 


The  Development  of  the  Frog      29 

dorsal  lip  of  the  blastopore  has  first  appeared,  and  even 
just  prior  to  that  time.  The  innermost  of  those  cells 
forming  the  ring  around  the  egg  are  the  cells  that  become 
the  mesoderm.  These  cells  are  carried  up  to  the  median 
dorsal  line  of  the  embryo  by  the  closure  of  the  blasto- 
pore. They  will  then  be  found  forming  a  layer  or  sheet 
of  cells  that  separates  itself  on  the  outer  side  from  the 
thick  layer  of  small  ectodermal  cells  (that  has  been  simul- 
taneously lifted  up)  and  that  is  separated  on  the  inner 
surface,  but  not  very  sharply,  if  at  all,  from  the  dorsal 
and  dorso-lateral  walls  of  the  archenteron." 

This  layer  of  mesoblast,  lying  between  the 
ectoblast  above  and  the  entoblast  below,  is  de- 
scribed by  Morgan  as  being  continuous  across 
the  dorsal  side  of  the  embryo,  but  it  is  more 
often  said  to  consist  of  two  lateral  portions,  sep- 
arated along  the  mid-dorsal  line  by  the  noto- 
chord,  which  is  formed  at  about  the  same  time. 

The  two  plates  of  mesoblast  rapidly  extend 
towards  the  mid-ventral  line,  where  they  fuse 
and  thus  form  a  continuous  layer  under  the 
ectoblast  (Figs.  10  and  13). 

Soon  after  its  formation  as  a  distinct  layer, 
the  mesoblast  separates,  beginning  on  each 
side  of  the  notochord,  into  two  layers,  one 
lying  next  to  the  ectoblast  and  known  as  the 
somatopleure,  and  one  lying  next  the  ento- 
blast, or  yolk,  and  known  as  the  splanchno- 


30  Vertebrate  Embryology 

pleure.  The  space  left  between  its  two  layers 
by  this  cleavage  of  the  mesoblast  will  become 
the  body-cavity,  or  ccelom  (Figs.  13,  C,  and  15). 
As  the  yolk-plug  is  withdrawn  within  the  egg, 
the  lateral  lips  of  the  blastopore  come  together 
to  form  a  slight  ridge  or  streak  of  tissue,  the 
primitive  streak,  in  the  centre  of  which  is  a 
narrow  chink  or  groove,  the  primitive  groove 

A  B  C  T>  E 


Tip 

FIG.  ii. — STAGES  IN  THE  EARLY  DEVELOPMENT  OF  THE  FROG, 

SEEN    OBLIQUELY  FROM   THE   POSTERIOR   END.       (After  Zleglcr,  from 

Marshall.) 

AI  yolk-plug  stage.  B,  primitive  streak  and  early  neural  folds.  C,  later 
neural  folds.  Z>,  closure  of  neural  canal  and  beginning  of  tail.  £,  completion  of 
neural  tube,  closure  of  blastopore,  presence  of  proctodaeum,  increase  in  tail. 

(Fig.  u,  B,  C,  and  D).  The  primitive  streak 
is  very  inconspicuous  in  the  frog,  but,  as  will 
be  seen  later,  in  the  chick  it  is  a  very  clearly 
defined  structure. 

Fate  of  the  Germ-Layers 

From  the  three  germ-layers,  whose  origins 
have  been  briefly  discussed,  are  derived  all  of 
the  organs  of  the  body. 


The  Development  of  the  Frog      31 

From  the  ectoblast  are  derived  the  epidermis 
and  the  various  structures  derived  from  the 
epidermis,  such  as  hairs,  nails,  etc.;  the  central 
and  peripheral  nervous  systems ;  parts  of  the 
eye,  ear,  and  nose ;  the  lining  of  the  mouth 
and  anus ;  and  the  pineal  gland  and  pituitary 
body. 

From  the  entoblast  are  derived  the  lining 
epithelium  of  the  digestive  tract,  with  all  its 
diverticula,  such  as  lungs,  liver,  etc.;  and  the 
notochord  ;  though  there  is  some  difference  of 
opinion  as  to  the  origin  of  the  latter  structure. 

From  the  mesoblast  are  derived  all  of  the 
other  organs  of  the  body,  such  as  bones, 
muscles,  blood,  blood-vessels,  and  uro-genital 
organs. 

The  development  of  the  more  important 
organs  of  the  body  will  now  be  described,  and 
it  will  be  best  to  complete  the  discussion  of 
each  organ  in  turn,  rather  than  to  attempt  to 
describe  their  synchronous  development. 

DEVELOPMENT  OF  THE  NERVOUS  SYSTEM 

Since  the  nervous  system  is  one  of  the  first 
to  make  its  appearance  in  the  frog,  as  well  as 
in  other  animals,  it  is  a  convenient  one  with 
which  to  begin  the  discussion. 


32  Vertebrate  Embryology 

The  ectoblast,  formed,  as  has  been  described, 
by  the  gradual  spreading  of  the  pigmented 
cells  over  the  entire  egg,  soon  shows  two  more 
or  less  distinct  layers,  an  outer  or  epidermal, 
and  an  inner  or  nervous  layer  (Fig.  9). 

At  about  the  time  of  the  closure  of  the  blas- 
topore,  when  the  embryo  is  still  almost  spher- 
ical in  shape  (Fig.  n,  /?),  the  nervous  layer 
thickens  to  form  the  neural  plate,  which  extends 
along  the  dorsal  side  of  the  embryo,  and  causes 
it  to  be  slightly  flattened.  The  neural  plate 
at  its  posterior  end,  which  is  just  above  the 
blastopore,  is  narrow,  but  it  gradually  widens 
as  it  extends  forward  for  about  one  third  of 
the  circumference  of  the  embryo.  The  edges 
of  the  neural  plate  soon  begin  to  thicken  and 
to  be  elevated  slightly  on  all  sides,  forming 
the  neural  folds ;  and  the  neural  groove  is 
formed  as  a  shallow  furrow,  extending  forward 
from  the  blastopore  along  the  middle  of  the 
neural  plate  (Fig.  i,  /  and  /,  and  Fig.  n,  B 
and  C). 

The  neural  folds  (Fig.  13,  NF)  become 
more  and  more  elevated  until  they  meet  and 
fuse  along  the  mid-dorsal  line,  converting  the 
neural  groove  into  a  closed  tube,  the  neural 
canal  (Fig.  15,  NS).  The  fusion  of  the  neural 


BM 


BF 


A  L 

FIG.  12.    A. — SAGITTAL  SECTION  OF  EMBRYO  SHOWN  IN  FIG.  n, 

D,    SHORTLY    BEFORE    THE    CLOSURE   OF   THE   BLASTOPORE.       (After 

Marshall.) 

B,  blastopore.  B F,  fore-brain.  B  H,  hind-brain.  BM,  mid-brain.  //, 
entoblast.  L,  liver.  M.  mesoblast.  MN,  mesenteron.  N,  notochord.  7VC, 
neurenteric  canal.  /*,  beginning  of  pituitary  body  as  in  growth  of  ectoblast. 
PD)  proctodseum.  /?,  rectal  diverticulum  of  mesenteron.  6",  central  canal  of 
spinal  cord.  F,  yolk-cells. 

B. — SAGITTAL  SECTION  OF  EMBRYO  SHOWN  IN  FIG.  ir,  E,  SHORTLY 

AFTER  THE  CLOSURE  OF  THE  BLASTOPORE.       (After  Marshall.) 

BF,  fore-brain.  B H,  hind-brain.  BM,  mid-brain.  CH}  notochord.  M, 
mesoblast.  N  C,  neural  tube.  N  T,  neurenteric  canal.  PN,  pineal  body.  P  T, 
pituitary  body.  T  I,  intestinal  region  of  mesenteron.  TP,  pharyngeal  region  of 
mesenteron.  U,  proctodseal  or  cloacal  opening.  W,  liver.  J-',  yolk-cells. 

33 


34  Vertebrate  Embryology 

folds  begins  in  what  will  be  the  neck  region  of 
the  future  tadpole,  and  extends  forward  and 
backward  from  that  point,  the  extreme  anterior 
end  being  the  last  to  close  in  completely.  As 
the  neural  folds,  or  medullary  folds  as  they 
are  often  called,  fuse  together  to  form  the 
neural  or  medullary  canal,  the  epidermal  layer 
of  ectoblast  fuses  over  the  top,  and  forms,  once 
more,  a  smooth,  continuous  layer  (Figs.  12 
and  15). 

It  will  be  seen  by  an  examination  of  the 
figures  that  the  chief  thickness  of  the  wall  of 
the  neural  tube  is  derived  from  the  nervous 
layer  of  ectoblast,  but  that  the  layer  of  cells 
which  lines  the  inside  of.  the  tube  is  from  the 
epidermal  layer  (Fig.  13). 

The  extreme  posterior  ends  of  the  neural 
folds  extend  on  each  side  of  the  blastopore,  so 
that,  as  they  come  together,  they  cover  the 
blastopore,  which  persists  for  a  time  as  a  nar- 
row passage,  the  neurenteric  canal,  connecting 
the  mesenteron  with  the  neural  canal  (Fig. 
12,  jVC  and  NT). 

The  neural  tube,  formed  as  above  described, 
becomes  converted  into  the  central  nervous 
system,  the  anterior  end  forming  the  brain,  the 
rest  of  the  tube  forming  the  spinal  cord. 


The  Development  of  the  Frog       35 

Of  the  changes  that  convert  the  simple  tube 
into  the  adult  cord  little  need  be  said.  The 
walls  thicken  rapidly,  and  the  originally  large, 
circular  canal  is  reduced  to  a  narrow,  vertical 
slit  (Fig.  15,  NS).  As  development  proceeds, 


NF 


ME 


MH 


FIG.  13. — TRANSVERSE  SECTION  THROUGH  A  FROG 
EMBRYO  DURING  THE  FORMATION  OF  THE  NEURAL 
CANAL.  (After  Marshall.) 

C,  coelom.  E  F,  epidermic  layer  of  ectoblast.  EN,  nervous 
layer  of  ectoblast.  H,  entoblast.  M,  mesoblast.  ME,  somato- 
pleuric  layer  of  mesoblast.  M  //,  splanchnopleuric  layer  of  meso- 
blast. M 'jV,  mesenteron.  N,  notochord.  N F,  neural  fold. 
N  G,  neural  groove.  K,  yolk-cells. 

the  relative  size  of  the  canal  becomes  smaller 
and  smaller  until,  in  the  adult,  it  is  seen  as 
a  tiny  tube  in  the  centre  of  the  cord,  lined 
with  a  thin  layer  of  epithelial  cells,  derived 


36  Vertebrate  Embryology 

from  the  epidermal  layer  of  the  original  ecto- 
blast. 

The  changes  that  convert  the  anterior  end 
of  the  neural  tube  into  the  complicated  struc- 
tures of  the  adult  brain  are  much  more  exten- 
sive, and  must  be  described  in  more  detail, 
although  the  limits  of  this  work  will  not  per- 
mit a  full  description. 

The  first  indication  of  a  separation  of  the 
brain  from  the  rest  of  the  neural  tube  is  seen 
at  about  the  time  of  the  appearance  of  what  is 
known  as  cranial  flexure.  As  the  name  would 
indicate,  cranial  flexure  is  the  bending  of  the 
brain,  at  about  its  middle  region,  so  that  the 
anterior  end  is  pushed  down,  and  comes  to 
lie  almost  at  right  angles  with  the  posterior 
part  (Fig.  12). 

This  cranial  flexure  takes  place  around  the 
anterior  end  of  the  notochord,  and  persists 
throughout  life,  its  apparent  rectification  being 
due  to  inequalities  in  the  growth  of  the  differ- 
ent parts  of  the  brain.  At  this  time  the  cen- 
tral nervous  system  has  somewhat  the  shape 
of  a  retort,  the  bulb  of  the  retort  corresponding 
to  the  brain,  and  the  neck  of  the  retort  cor- 
responding to  the  spinal  cord. 

Two  transverse  folds  appear  very  early  in 


The  Development  of  the  Frog      37 

the  brain  region,  dividing  it  into  three  more  or 
less  distinctly  marked  portions,  the  fore-brain, 
mid-brain,  and  hind-brain  (Fig.  12.)  The  de- 
velopment of  these  regions  of  the  brain  will  be 
taken  up,  briefly,  in  turn. 

The  hind-brain  forms  the  medulla  and  cere- 
bellum of  the  adult,  its  cavity  remaining  as  the 
fourth  ventricle.  The  floor  and  sides  of  the 
hind-brain  become  thickened,  while  the  roof 
becomes  very  thin,  except  at  the  part  next  to 
the  mid-brain,  where  the  cerebellum  is  devel- 
oped (Fig.  1 6). 

The  floor  of  the  mid-brain  thickens  to  form 
the  crura  cerebri,  while  from  the  roof  grow 
out  two  hollow,  ovoid  bodies,  the  optic  lobes. 
The  cavity  of  the  mid-brain  persists  as  the 
Sylvian  aqueduct  or  tier. 

The  walls  of  the  fore-brain  (thalamenceph- 
alon  of  the  adult)  thicken  to  form  the  optic 
thalami  and  its  cavity,  the  third  ventricle,  is 
thus  reduced  to  a  narrow,  vertical  slit.  From 
the  floor  of  the  fore-brain  the  infundibulum  is 
formed  as  a  hollow  pouch,  pushed  out  in  a 
ventro-posterior  direction  (Figs.  14,  IN,  1 7,  and 
1 8,  /).  Since  the  pituitary  body  is  so  closely 
associated  with  the  infundibulum,  its  origin 
will  be  spoken  of  at  this  time. 


38  Vertebrate  Embryology 

At  a  very  early  period,  a  thickening  of  the 
nervous  layer  of  the  ectoblast  is  formed  just 
below  the  anterior  end  of  the  neural  canal.  This 
collection  of  cells  grows  inward  as  a  tongue 
of  ectoblast  tissue  between  the  anterior  end  of 
the  brain  and  the  digestive  tract  (Figs.  14,  PT, 
17,  and  1 8,  P).  The  inner  end  of  this  tongue 
of  cells  becomes  broader  and  hollow,  and  even- 
tually separates  from  its  stalk  to  form  the 
pituitary  body,  which  lies  just  under  the  in- 
fundibulum  (Fig.  18,  /).  From  the  roof  of 
the  fore-brain,  at  the  point  where  the  neural 
tube  finally  closed,  a  small,  hollow  diverticu- 
lum  is  pushed  out  and  becomes  enlarged  at 
the  end  (Figs.  14  and  17,  7W).  This  is  the 
pineal  body,  and  when  the  skull  is  formed  it 
cuts  off  the  enlarged  knob  from  its  hollow 
stalk,  the  knob,  which  has  become  solid,  re- 
maining outside  of  the  skull,  and  the  stalk 
retaining  its  connection  with  the  fore-brain. 

The  cerebral  hemispheres,  which  form  the 
larger  part  of  the  fore-brain,  do  not  form  until 
a  comparatively  late  period.  They  begin  as  a 
large,  median  diverticulum  from  the  front  of 
the  fore-brain  (Figs.  17,  CV,  and  18),  which 
diverticulum  is  at  first  unpaired,  but  later  be- 
comes divided  into  the  two  hemispheres. 


<n  ^ 


40  Vertebrate  Embryology 

The  olfactory  lobe  is  formed  by  the  fusion 
of  an  outgrowth  from  the  anterior  end  of 
each  cerebral  hemisphere.  The  cerebral  hem- 
ispheres are  at  first  unpaired  and  later  become 
double,  while  the  olfactory  lobe  is  at  first 
double  and  afterwards  becomes  single. 

There  are  many  details  in  the  development 
of  the  peripheral  nervous  system  that  are  not 
yet  clearly  understood.  The  dorsal  roots  of 
the  spinal  nerves  arise  very  early  as  outgrowths 
from  the  sides  of  the  neural  plates  before  the 
latter  fuse  together  to  form  the  neural  canal. 
They  grow  down  between  the  neural  canal 
and  the  myotornes  (Fig.  15,  ND)  and  become 
slightly  enlarged,  a  short  distance  from  their 
points  of  origin,  to  form  the  spinal  ganglia. 
The  ventral  roots  of  the  spinal  nerves  arise 
later  as  independent  outgrowths  from  the  ven- 
tral side  of  the  neural  canal,  and  fuse  with  the 
dorsal  roots  distal  to  the  spinal  ganglia. 

DEVELOPMENT  OF  THE  SENSE  ORGANS 

Since  the  organs  of  special  sense  are  chiefly 
derived  from  the  ectoblast,  and  since  they 
are  all  closely  connected  with  the  brain,  it 
is  well  to  speak  of  their  development  at  this 
point. 


The  Development  of  the  Frog      41 

THE  EYE 

The  development  of  the  eye  can  be  more 
easily  made  out  in"  the  chick  than  in  the  frog, 


NS 


M 


FIG.  15. — TRANSVERSE  SECTION  ACROSS  THE  MIDDLE  OF  THE 
EMBRYO  SHOWN  IN  FIG.  II,  D.     (After  Marshall.) 

CH,  notochord.  C/,  subnotochordal  rod.  CM,  myocoel.  CS,  body  cav- 
ity. E,  ectoblast.  KB,  archinephric  duct.  M,  mesoblast.  MS,  mesoblastc 
somite.  ND,  dorsal  root  of  spinal  nerve.  N S,  spinal  cord.  .S  0,  somatopleure. 
SP,  splanchnopleure.  T,  intestinal  region  of  mesenteron.  F,  yolk-celJs. 

so  that  many  of  the  details  will  be  left  until 
the  latter  part  of  the  book,  since  the  process 
is  essentially  the  same  in  both  animals. 

The  first  rudiment   of   the  eye   is  seen   in 


42  Vertebrate  Embryology 

very  young  tadpoles  as  an  evagination  from 
each  side  of  the  fore-brain.  This  evagination, 
which  is  known  as  the  optic  vesicle,  reaches  a 
considerable  size  and  becomes  constricted  off 
from  the  brain,  so  that  it  forms  a  large,  hollow 
bulb  connected  with  the  brain  by  a  very  nar- 
row stalk. 

The  walls  of  the  optic  vesicle  are  at  first 
comparatively  thin,  but  as  the  vesicle  enlarges 
and  approaches  the  superficial  ectoblast,  the 
wall  of  the  vesicle  that  is  next  to  the  ectoblast 
begins  to  thicken  and  at  the  same  time  to  be 
pushed  in  on  itself  (Fig.  19,  OC);  this  in  vagi- 
nation  of  the  optic  vesicle  continues  until  the 
two  walls  are  in  contact,  and  the  cavity  of  the 
original  optic  vesicle  is  obliterated.  The  cup- 
shaped  structure  which  is  thus  formed,  and 
which  is  still  connected  with  the  fore-brain  by 
the  narrow  stalk,  is  known  as  the  optic  cup. 
The  thick  inner  wall  of  the  optic  cup  forms 
the  essential  part  of  the  retina,  while  the  thin 
outer  wall  forms  the  pigmented  layer  that  sur- 
rounds the  retina.  The  rim  of  the  optic  cup 
is  not  complete,  like  the  rim  of  an  invaginated 
hollow  rubber  ball,  but  is  interrupted,  at  one 
place,  as  a  narrow  slit  known  as  the  choroid 
fissure.  Through  the  choroid  fissure  the  sur- 


The  Development  of  the  Frog      43 

rounding  mesoblast  enters  the  optic  cup  and 
forms  the  vitreous  humor.  The  outer  layers  of 
the  eye  are  formed  from  the  mesoblast.  As  the 
optic  vesicles  approach  the  superficial  ectoblast, 
the  inner  layer  of  the  latter  becomes  thickened, 
and  eventually  separates  from  the  outer  layer 
and  lies  at  the  opening  of  the  optic  cup  as  a 
hollow  spherical,  or  ovoid  body,  the  lens  vesicle 
(Figs.  19,  OL,  and  20  OL).  By  the  growth  of 
its  walls,  chiefly  the  inner,  the  cavity  of  the 
lens  vesicle  is  obliterated  and  the  adult  lens  is 
formed. 

THE  EAR 

The  ear  begins  as  a  thickening,  followed  by 
an  invagination  of  the  inner  or  nervous  layer 
of  the  ectoblast.  This  invagination  begins  very 
early  and,  in  the  frog,  never  opens  to  the  ex- 
terior. It  is,  almost  from  the  first,  connected 
with  the  brain  by  the  auditory  nerve.  The 
invagination  gradually  closes  to  form  a  com- 
paratively thin-walled  cavity,  lying  in  the  re- 
gion of  the  hind-brain,  known  as  the  auditory 
vesicle.  This  vesicle,  whose  walls  are  com- 
posed of  a  single  layer  of  cells  (Fig.  21,  E), 
forms  the  lining  of  the  middle  ear.  A  more 

o 

complete  description  of  the  development  of  the 
ear  will  be  given  in  connection  with  the  chick. 


44  Vertebrate  Embryology 

THE  NOSE 

The  nose,  like  the  eye  and  ear,  begins  at  a 
very  early  period,  and  is  first  seen  as  two 
thickenings  of  the  inner  layer  of  the  ectoblast, 


FIG.  16. — THE  BRAIN  OF  THE  FROG.     (After  Marshall.)     Figure 
on  left  is  a  dorsal  view  ;  figure  on  right  is  a  ventral  view. 

C,  cerebellum.  CH,  cerebral  hemisphere.  CP,  choroid  plexus  of  third  ven- 
tricle. F)  fourth  ventricle.  IN,  tuber  cinereum.  M,  medulla  oblongata.  O, 
olfactory  lobe.  O  C,  optic  chiasma.  O  L,  optic  lobe.  /*,  stalk  of  pineal  body. 
P  B,  pituitary  body.  T,  thalamencephalon. 

/,  olfactory  nerve.  //,  optic  nerve.  ///,  third  or  motor  oculi  nerve.  IV, 
fourth  nerve.  V,  fifth  or  trigeminal  nerve.  VI \  sixth  nerve.  VII  and  VIII, 
combined  root  of  facial  and  auditory  nerves.  IX  and  X,  combined  root  of  glosso- 
pharyngeal  and  pneumogastric  nerves. 

one  on  each  side  of  the  anterior  end  of  the 
head.  An  in  vagination  of  both  layers  of  the  ecto- 
blast now  takes  place  (Fig.  22,  OF),  forming 
the  nasal  pits  whose  openings  to  the  exterior 


The  Development  of  the  Frog      45 

will  form  the  anterior  nares.  The  lining  of 
the  nasal  pits  will  become  connected  with  the 
brain  by  the  olfactory  nerves,  and  will  form 
the  olfactory  epithelium  of  the  nose.  From 
the  inner  side  of  the  nasal  pits  a  diverticulum 
grows  down  to  open  into  the  mouth  cavity  as 
the  posterior  nares. 

DEVELOPMENT  OF  THE  ALIMENTARY  TRACT 

The  origin  of  the  primitive  digestive  tract 
or  archenteron  has  already  been  given  :  it  now 
remains  to  describe  the  further  changes  that 
take  place  in  the  digestive  tract  itself,  and  to 
describe  the  development  of  the  various  struc- 
tures that  are  derived  from  it. 

The  digestive  tract  may,  for  convenience, 
be  divided  into  three  regions:  (i)  the  mesen- 
teron  (whose  formation  has  been  described), 
which  is  lined  with  entoblast  and  from  which 
are  developed  the  liver,  pancreas,  lungs,  gill 
clefts,  etc.  ;  (2)  the  stomodczum,  which  forms 
the  mouth  ;  (3)  the  proctodceum  or  cloacal  re- 
gion. The  first  region  is  lined  throughout 
with  entoblast,  while  the  latter  two  are  both 
lined  with  ectoblast.  The  reason  for  this  dif- 
ference will  be  seen  when  the  development  of 
the  mouth  and  anus  is  described. 


46  Vertebrate  Embryology 

The  anterior  end  of  the  digestive  tract  early 
becomes  expanded  into  what  may  be  called 
the  pharynx,  and  there  is  a  similar  though 
smaller  expansion  at  the  posterior  end  (Figs. 
12  TP  and  22).  The  entoblast  at  first  forms 
a  more  distinct  layer  on  the  dorsal  side  of  the 
mesenteron  than  it  does  on  the  ventral  side, 
but  it  very  soon  extends  entirely  around  the 
cavity  as  a  distinct  layer. 

In  the  frog  the  primitive  mouth  or  blastopore 
closes  entirely,  so  that  the  digestive  tract  may 
be  for  a  short  time  a  completely  closed  cavity, 
but  in  some  other  animals  the  blastopore  per- 
sists as  the  permanent  anus. 

Shortly  before  hatching,  a  depression  of  the 
ectoblast  may  be  seen  on  the  ventral  side  of 
the  head  (Fig.  14,  DS}  ;  this  is  the  beginning 
of  the  stomodaeum.  The  depression  becomes 
deeper  and  deeper  until  it  is  separated  from 
the  front  of  the  pharynx  by  only  a  thin  septum 
(Fig.  17,  S  D).  Soon  after  hatching  this  sep- 
tum becomes  perforated  and  the  mouth  open- 
ing is  formed.  The  lips  now  grow  forward, 
the  jaws  become  formed,  and  the  tadpole 
begins  to  take  food  from  the  surrounding 
water  (Fig.  18). 

The  proctodaeum  or  anal  opening  is  formed 


The  Development  of  the  Frog      47 

before   the   stomodaeum.      Before  the    neural 
canal  has  been  completely  closed  a  small  de- 


PN 


so 


FIG.  17. — LONGITUDINAL  VERTICAL  SECTION  THROUGH  THE  AN- 
TERIOR END  OF  A  TADPOLE  SHORTLY  AFTER  THE  TIME  OF  HATCHING. 

LENGTH  OF  THE  TADPOLE,  8  MM.     (After  Marshall.) 

A,  auricle  of  heart.  B F,  fore-brain.  BH,  hind-brain.  B M*  mid-brain. 
C',  pericardia!  cavity.  C  V,  vesicle  of  cerebral  hemispheres.  /,  infundibulum. 
Z,,  liver.  jV,  notochord.  O,  depression  of  floor  of  fore- brain  from  which  the 
optic  vesicles  arise.  O £,  oesophagus.  P,  pituitary  body.  P N,  pineal  body. 
S,  central  canal  of  spinal  chord.  SD,  stomodaeum.  7',  truncus  arteriosus.  Vy 
ventricle.  I",  yolk-cells. 

pression  is  seen  below  the  blastopore  (Fig.  1 2, 
PD)  ;  this  is  the  beginning  of  the  anal  in- 
vagination.  At  the  same  time  a  diverticulum 


48  Vertebrate  Embryology 

grows  backward  from  the  posterior  end  of  the 
digestive  tract  towards  this  invagination  (Fig. 
12),  with  which  it  finally  fuses  and  thus  puts 
the  hind  gut  in  communication  with  the  ex- 
terior (Figs.  12  £/,  and  14,  £/).  The  formation 
of  the  proctodaeum  may  be  completed  before 
the  closure  of  the  blastopore,  so  that  the  hinder 
end  of  the  digestive  tract  may  have  two  open- 
ings to  the  exterior. 

It  will  be  understood,  from  the  above  de- 
scription, why  it  is  that  the  oral  and  anal 
cavities  are  lined  with  ectoblast  instead  of 
with  entoblast,  as  is  the  rest  of  the  digestive 
canal. 

The  liver  may  be  early  recognized  as  a  diver- 
ticulum  pushed  out  from  the  front  end  of  the 
digestive  tract  in  a  ventro-posterior  direction 
(Figs.  12  and  14,  W}.  The  walls  of  this 
diverticulum  thicken  and  become  folded,  and 
the  mesoblast  penetrates  between  these  folds. 
The  diverticulum,  which  is  evidently  lined 
with  entoblast,  persists  as  the  bile  duct,  and 
from  it  an  outgrowth  arises  to  form  the  gall 
bladder. 

The  pancreas  arises  as  a  pair  of  hollow  out- 
growths from  the  mesenteron  back  of  the 
liver. 


The  Development  of  the  Frog      49 

The  lungs  arise  from  the  narrow  part  of  the 
digestive  tract  which  lies  just  back  of  the  wide 
anterior  end  or  pharynx.  A  longitudinal  fold 


CH 


FIG.  18. — LONGITUDINAL  VERTICAL  SECTION  THROUGH  THE  HEAD 
AND  ANTERIOR  PART  OF  THE  BODY  OF  A  TADPOLE  ABOUT  THE  TIME 
OF  APPEARANCE  OF  THE  HIND  LEGS.  LENGTH  OF  TADPOLE,  12  MM. 
X  14.  (After  Marshall.) 

A,  auricle  of  heart.  A  Z>,  dorsal  aorta.  B B,  basi-branchial  cartilage.  B Fy 
fore-brain.  B  H,  hind-brain.  B  M^  mid-brain.  C,  coelom  or  body-cavity.  C', 
pericardial  cavity.  C H,  cerebral  hemisphere.  CB.  rudimentary  cerebellum. 
CP,  choroid  plexus  of  fourth  ventricle.  CP\  choroid  plexus  of  third  ventricle. 
7%  pharynx.  G,  stomach.  //,  lung.  7,  infundibulum.  J,  horny  jaws,  /f,  lip. 
L,  liver.  A",  notochord.  O,  depression  of  floor  of  fore-brain  from  which  the 
optic  nerves  arise.  OE,  oesophagus.  P,  pituitary  body.  PN^  pineal  body.  S1, 
central  canal  of  spinal  chord.  7",  truncus  arteriosus.  V,  ventricle. 

appears  in  each  side  of  the  mesenteron,  at  this 
place,  and  by  the  meeting  of  these  folds  the 
digestive  tract  is  divided  into  a  dorsal  portion 


50  Vertebrate  Embryology 

or  oesophagus,  and  a  ventral  portion  or  larynx. 
From  the  laryngeal  chamber  the  lungs  arise 
as  hollow  lateral  outgrowths,  some  time  after 
hatching,  when  the  tadpole  is  about  8  mm. 
long.  At  about  the  time  of  the  formation  of  the 
lungs  the  tubular  oesophagus  becomes  solid 
and  remains  closed  until  after  the  formation 
of  the  oral  opening.  What  the  significance  of 
this  curious  fact  may  be  is  not  known. 

The  thyroid  body  begins,  at  about  the  time 
of  hatching,  as  a  small,  median  depression  in  the 
floor  of  the  pharynx.  The  depression  becomes 
deeper,  especially  at  its  posterior  end,  and 
finally  loses  its  connection  with  the  pharynx 
and  lies  as  a  solid  rod  of  cells  just  in  front  of 
the  pericardium.  When  the  tadpole  is  about 
1 2  mm.  in  length  the  thyroid  becomes  sepa- 
rated into  right  and  left  halves  by  the  growth 
of  a  median  longitudinal  septum,  and  after 
considerable  growth  each  of  these  halves  is 
converted  into  the  adult  structure  by  the  re- 
arrangement of  its  cells  to  form  the  round  or 
oval  vesicles  that  are  characteristic  of  the  thy- 
roid gland. 

The  bladder  arises  at  about  the  time  of 
metamorphosis  as  an  outgrowth  from  the  ven- 
tral wall  of  the  hind  gut. 


The  Development  of  the  Frog      5 1 

DEVELOPMENT   OF   THE   GILL  CLEFTS   AND 

FOLDS 

The  gill  clefts  are  five  pairs  of  narrow, 
vertical  slits  which  connect  the  cavity  of  the 
pharynx  with  the  exterior.  The  portions  of 
the  wall  between  the  clefts,  and  also  in  front 
of  the  first  and  behind  the  last  clefts  are  the 
gill  folds  or  arches.  The  most  anterior  cleft  is 
known  as  the  hyomandibular  cleft,  the  others, 
from  before  back,  are  the  first,  second,  third, 
and  fourth  gill  clefts.  The  arch  in  front  of  the 
hyomandibular  cleft  is  called  the  mandibular 
arch,  the  arch  between  the  hyomandibular  and 
the  first  gill  clefts  is  the  hyoid  arch,  and  the 
other  arches,  like  the  clefts,  are  called  the  first, 
second,  third,  and  fourth. 

The  gill  clefts,  or,  as  they  are  often  called, 
the  visceral  or  branchial  clefts  or  pouches,  be- 
gin to  develop  before  the  tadpole  hatches,  and 
are  best  studied  in  horizontal  sections.  The 
first  three  pairs  of  pouches  begin  almost  simul- 
taneously as  evaginations  of  the  entoblastic 
wall  of  the  pharynx,  which  push  outward 
towards  the  ectoblast.  The  third  and  fourth 
pouches  are  formed  in  succession  behind  the 
first  three.  All  of  the  pouches  grow  outward 
until  they  come  in  contact  with  the  ectoblast, 


52  Vertebrate  Embryology 

with  whose  inner  layer  they  fuse  (Fig.  22). 
The  two  lamellae  of  entoblast  that  make  up 
the  pouches  are  at  first  in  contact  with  each 
other,  so  that  there  is  no  actual  cleft  between 
them  (Fig.  22,  HM,  HC.\)  ;  but  at  about  the 
time  of  the  opening  of  the  mouth  the  lamellae 


FIG.  19. — HALF  SECTIONS  IN  THE  TRANSVERSE  PLANE 

OF   A  TADPOLE,  IO  MM.  LONG  (LEFT  HALF)   AND   OF  A 
TADPOLE   12   MM.  LONG  (RIGHT  HALF).       X  35-      (After 

Marshall.) 

B  F,  fore-brain.  O  Z>,  outer  wall  of  optic  cup  (pigment  layer 
of  adult  retina) ;  O  C,  inner  wall  of  optic  cup  (remainder  of  adult 
retina).  O Z.,  lens,  attached  to  epiblast  in  younger  tadpole,  but 
forming  a  hollow  vesicle  at  the  later  stage.  TP.  pharynx.  O. 
sucker.  [G.  H.  F.] 

separate  from  each  other  to  form  the  actual 
clefts,  all  of  which  open  to  the  exterior  except 
the  hyomandibular  pair,  which  recede  from 
the  ectoblast  and  persist,  for  a  time,  as  a 
pair  of  diverticulae  from  the  front  part  of  the 
pharynx. 


The  Development  of  the  Frog      53 

The  Eustachian  tube  and  the  tympanic  cav- 
ity develop  near  the  hyomandibular  cleft,  but 
it  is  doubtful  if  any  such  close  relation  exists 
between  those  structures  and  the  hyomandib- 
ular cleft  as  exists  in  some  other  animals. 

The  other  visceral  clefts  persist  for  a  con- 
siderable time,  but  towards  the  end  of  the 
tadpole  stage  they  close  up  and  disappear. 

The  fate  of  the  gill  arches  is  of  more  im- 
portance, but  as  it  is  more  easily  studied  in 
the  chick,  a  very  brief  statement  will  suffice  at 
this  time.  The  mandibular  arch,  as  its  name 
would  indicate,  becomes  converted  into  the 
essential  part  of  the  lower  jaw.  The  hyoid 
arch,  as  its  name  indicates,  forms  the  greater 
part  of  the  hyoid  apparatus,  while  the  other 
four  arches  almost  entirely  disappear.  Dur- 
ing the  larval  period  there  is  present  in  each 
visceral  arch  a  rod  of  cartilage,  which  is  closely 
joined  to  its  fellow  of  the  opposite  side  ven- 
trally  but  is  separated  from  it  dorsally.  Thus 
there  is  in  each  pair  of  arches  a  U-shaped  bar 
of  cartilage  which  serves  to  stiffen  the  walls  of 
the  pharynx. 

The  gills,  of  which  there  are  two  sets,  the 
external  and  the  internal,  are  developed  in 
connection  with  the  gill  arches. 


54 


Vertebrate  Embryology 


Even  before  the  tadpole  is  hatched  there 
may  be  seen,  on  each  side  of  the  neck  region,  a 
series  of  vertical  folds,  or  thickenings ;  these 
are  the  visceral  folds,  and  it  is  upon  them  that 


OL 


OS 


PT 


TP 


FIG.  20. —  TRANSVERSE  SECTION  THROUGH  THE 
HEAD  OF  A  TADPOLE  6^  MM.  IN  LENGTH  ABOUT  THE 
TIME  OF  HATCHING,  THE  SECTION  PASSING  THROUGH 

THE     FORE  -  BRAIN     AND     DEVELOPING     EYES.        (After 

Marshall.) 

A  C  carotid  artery.  B  F.  fore-brain.  DS,  stomodaeal  pit. 
NL,  cutaneous  or  lateral  line  branch  of  trigeminal  nerve.  O  C, 
inner  wall  of  optic  cup.  O  D,  outer  wall  of  optic  cup.  O  L,  lens. 
OS,  optic  stalk.  PT,  pituitary  body.  TP,  pharynx.  VJ, 
jugular  vein. 

the  gills  are  developed  (Figs,  i,  K-O,  and  22). 
The  external  gills  appear  first,  reach  their 
maximum  development,  and  then  are  replaced 
by  the  internal  gills.  The  external  gills  arise, 
shortly  before  hatching,  upon  the  first  and 


The  Development  of  the  Frog      55 

second  gill  arches,  and  a  little  later  a  third 
pair  is  formed  upon  the  third  arch.  The  ex- 
ternal gills  reach  their  greatest  development 
at  about  the  time  of  the  opening  of  the  mouth, 
and  at  that  time  each  of  the  first  two  consists 
of  from  five  to  seven  main  lobes,  with  numer- 
ous secondary  lobes  along  their  posterior  bor- 
ders (Fig.  23,  A).  The  gills  on  the  third  arch 
are  much  smaller  than  those  of  the  arches  in 
front,  and  are  nearly  covered  by  them.  The 
course  of  the  circulation  in  the  external  gills 
may  be  easily  seen  under  the  microscope,  each 
main  lobe  and  each  minor  lobe  being  supplied 
with  an  efferent  and  an  afferent  blood-vessel 
(Fig.  23,  EF  and  AF). 

The  opercular  folds  arise,  before  the  mouth 
opens,  as  two  folds  of  skin  from  the  hyoid 
arches ;  they  unite  with  each  other  in  the  ven- 
tral line,  and  grow  backward  as  a  sort  of  hood 
over  the  external  gills  (Figs,  i,  O,  and  24).  The 
posterior  border  of  this  hood  fuses  with  the 
body  wall  behind  the  gills,  on  the  right  and 
ventral  sides,  but  remains  open  on  the  left  side 
as  a  sort  of  spout  (Fig.  24,  OA),  through 
which  the  gills  of  that  side  frequently  protrude, 
and  through  which  the  water,  taken  into  the 
gill  chamber  through  the  mouth,  passes  again  to 


56  Vertebrate  Embryology 

the  exterior.  The  opercular  folds  are  not  com- 
pleted until  after  the  formation  of  the  mouth. 

The  internal  gills  arise  quite  early  as  a 
double  row  of  papillae  on  the  first,  second,  and 
third  visceral  arches,  below  the  external  gills, 
and  as  a  single  row  on  the  fourth  arch.  They 
are  very  vascular,  and  when  the  external  gills 
begin  to  shrivel,  they  take  up  the  function  of 
respiration.  The  inner  borders  of  the  gill 
arches  develop  a  sort  of  straining  apparatus, 
to  prevent  solid  substances  from  passing  from 
the  pharynx  into  the  gill  chamber. 

At  the  end  of  the  tadpole  life,  as  the  lungs 
begin  to  function,  the  gill  chamber  is  filled  and 
gradually  obliterated  by  the  growth  of  lym- 
phoid  and  epithelial  tissue,  the  gill  clefts  are 
closed  by  the  fusion  of  their  edges,  and  the 
gills  are  almost  entirely  absorbed,  small  por- 
tions persisting  in  the  adult  as  the  so-called 
tonsils. 

THE    DEVELOPMENT    OF    THE     HEART    AND 
BLOOD  VESSELS 

As  has  been  stated  above,  the  heart  and 
blood  vessels,  as  well  as  the  blood  itself,  are 
formed  from  mesoblast,  the  chief  point  of  in- 
terest being  the  changes  that  take  place  at 


The  Development  of  the  Frog      57 

metamorphosis,  when  the  circulation  changes 
from  practically  that  of  a  fish  to  that  of  the 
adult  frog.  Since  changes  similar  to  these 


H,B. 


FIG.  21. — TRANSVERSE  SECTION  THROUGH  THE  RE- 
GION OF  THE  HIND-BRAIN  OF  A  YOUNG  TADPOLE. 

Z>,  digestive  tract.      E,  ear  vesicle.    H B^  hind-brain.      TV, 
note-chord.    St  sucker.     (Camera  lucida.) 

take  place  in  even  the  highest  animals,  they 
are  of  more  than  passing  interest. 

The  development  of  the  heart  and  pericar- 
dium, though  difficult  to  follow  out  in  detail  in 
the  laboratory,  will  be  readily  understood  from 
the  following  description,  studied  in  connection 
with  Fig.  25  : 


5  8  Vertebrate  Embryology 

"  The  heart  appears  at  the  time  when  the  medullary 
folds  have  rolled  in,  and  have  met  along  the  mid-dorsal 
line;  it  lies  below  the  pharynx,  and  anterior  to  the  liver 
(Fig.  12).  The  mesoderm  in  this  region  shows  a  tendency 
to  split  into  two  sheets,  and,  where  the  heart  is  about  to 
develop,  a  cavity,  a  part  of  the  ccelom,  appears  between 
the  sheets.  A  cross-section  of  the  larva  (Fig.  25,  A)  shows 
on  each  side  of  the  mid-ventral  line  in  the  region  of  the 
heart  the  somatic  and  splanchnic  layers  widely  separated 
from  each  other.  The  ccelomic  cavities  of  the  right  and 
left  sides  are  not  continuous  across  the  middle  line,  but 
anterior  and  posterior  to  this  section  the  ccelomic  cavity 
is  found  to  be  continuous  before  and  behind  with  the 
general  ccelomic  space  on  each  side.  A  few  scattered 
cells  lie  in  the  middle  line  between  the  splanchnic  layer 
and  the  wall  of  the  pharynx  (Fig.  25,  £).  These  cells  have 
been  described  as  originating  from  the  ventral  wall  of 
the  archenteron,  and,  if  so,  have  had  a  different  origin 
from  the  other  cells  of  the  heart. 

"  At  a  somewhat  later  stage  of  development  the  walls 
of  the  ccelomic  cavities  of  the  right  and  left  sides  sepa- 
rate further  (Fig.  25,  £).  The  splanchnic  layer  thickens, 
and  begins  to  surround  the  proliferation  of  scattered 
'endodermal  cells.'  These  endodermal  cells  arrange 
themselves  in  a  thin-walled  tube  stretching  throughout 
the  heart  region  (Fig.  25).  Subsequent  development 
shows  that  this  tube  becomes  the  endothelial  lining  of 
the  heart.  Around  this  endothelial  tube  the  thickened 
splanchnic  layers  now  begin  to  push  in  from  the  sides 
between  the  tube  and  the  lower  wall  of  the  pharynx. 
The  tube  becomes  finally  entirely  surrounded  by  meso- 
derm (Fig.  25).  The  mesoderm  from  the  sides  that  has 


6F 


OS 


BR.1 


BR.2 


KA 


KA 


FIG.  22.  —  HORIZONTAL  SECTION  OF  A  TADPOLE  AT  THE  TIME 
OF  HATCHING.     (After  Marshall.) 

A  F,  afferent  branchial  vessel  of  the  first  branchial  arch.  B  F,  fore-brain. 
B  R.I,  SR.2,  BR3,  first,  second,  and  third  branchial  arches.  C,  body-cavity  or 
coelom.  E  F,  efferent  branchial  vessel  of  first  branchial  arch.  H  M,  hyomandi- 
bular  gill-pouch.  H  K,  hy old  arch.  IN,  infundibulum.  KA,  archinephric  duct 
of  right  side.  KA',  archinephric  duct  of  left  side,  seen  in  section.  KP,  head- 
kidney  or  pronephros.  KS,  third  nephrostome  of  right  head-kidney.  KS',  same 
of  left  side,  seen  in  section.  OF,  olfactory  pit.  OS,  optic  stalk.  TP,  pharyn- 
geal  region  of  mesenteron.  TI,  intestinal  region  of  mesenteron.  V,  yolk-cells. 

59 


60  Vertebrate  Embryology 

met  beneath  the  pharynx  forms  the  dorsal  mesentery  of 
the  heart.  The  mesoderm  around  the  tube  continues  to 
thicken,  and  forms  later  the  musculature  of  the  heart. 

"  At  first  the  heart  has  also  a  ventral  mesentery  formed 
by  the  union  of  the  walls  of  the  coelomic  cavities  below 
it  (Fig.  25),  but  later  the  mesentery  is  in  part  absorbed 
and  the  coelomic  cavities  become  continuous  below  from 
side  to  side,  forming  the  pericardial  chamber.  The 
outer  layer  of  somatic  mesoderm  gives  rise  to  the  peri- 
cardium itself. 

"  The  tubular  heart  is  attached  at  its  posterior  end  to 
the  liver  and  anteriorly  to  the  wall  of  the  pharynx.  It 
becomes  free  ventrally  and  also  dorsally  along  the  middle 
of  its  course,  and  owing  to  an  increase  in  length  is  bent 
on  itself  into  an  co  -shaped  tube  (Fig.  14)."  1 

A  series  of  transverse  constrictions  now 
gives  indication  of  the  division  of  the  heart 
into  the  various  chambers,  though  there  are, 
for  a  time,  no  actual  partitions  between  the 
different  regions.  A  septum  is  finally  formed 
which  divides  the  single  auricle  into  right  and 
left  halves,  and  by  the  time  of  metamorphosis 
the  heart  has  practically  the  adult  structure. 

Without  distinguishing  between  the  exter- 
nal and  internal  gills,  the  larval  circulation  is, 
briefly,  as  follows :  "  The  venous  blood,  re- 
turned from  the  body  at  large,  enters  the  pos- 
terior end  of  the  heart,  or  sinus  venosus  ;  from 

1  Morgan. 


The  Development  of  the  Frog      61 

this  it  passes  into  the  second  or  auricular 
chamber,  thence  to  the  ventricle,  and  from  that 
to  the  truncus  arteriosus  (Fig.  17)."  As  there 
is,  at  first,  no  division  into  right  and  left  sides, 
the  blood  passes  in  succession  through  these 
various  chambers. 

"  The  truncus  arteriosus  divides  distally  into  right  and 
left  branches,  from  each  of  which  four  afferent  branchial 
vessels  (Fig.  26,  A  F,  1-4)  arise.  The  four  vessels  of 
each  side  run  outwards  along  the  hinder  borders  of  the 
four  branchial  arches,  giving  off  along  their  whole  length 
numerous  branches  to  the  gill-tufts  on  these  arches. 
From  the  gills  the  blood,  now  aerated,  passes  into  the 
efferent  branchial  vessels  (Figs.  23  and  26,  EF,  1-4). 
These  lie  alongside  of  the  afferent  branchial  vessels, 
and  just  in  front  of  them,  but  do  not  communicate  with 
them  except  through  the  capillary  loops  of  the  gills. 
The  four  efferent  branchial  vessels  of  each  side  unite  in 
the  dorsal  wall  of  the  pharynx  to  form  the  dorsal  aorta- 
the  two  aortae  are  continued  forwards  to  the  head  as  the 
carotid  arteries,  while  posteriorly  they  unite  to  form  the 
single  dorsal  aorta,  from  which  branches  arise  supplying 
all  parts  of  the  body  (Figs.  24,  A,  and  26,  A). 

The  lungs  arise  at  a  very  early  stage,  but  are  for  a  long 
time  extremely  small  and  of  little  functional  importance. 
Each  lung  receives  blood  from  a  branch  of  the  fourth  ef- 
ferent branchial  vessel  (Fig.  26,  AP),  and  returns  it  di- 
rectly to  the  auricle  by  \\\z  pulmonary  vein.  As  the  tadpole 
increases  in  size,  and  the  lungs  become  of  greater  im- 
portance, a  septum  appears,  dividing  the  auricle  into 


62  Vertebrate  Embryology 

systemic  or  venous,  and  pulmonary  or  arterial  cavities. 
Simultaneously  with  this,  valves  are  formed  in  the  trun- 
cus  arteriosus,  by  which  the  streams  of  venous  and  arte- 
rial blood  are  kept  apart  to  a  certain  extent.  At  the 
time  of  the  metamorphosis  the  gill  circulation  is  cut  off, 
by  the  establishment  of  direct  communications  between 
the  afferent  and  efferent  branchial  vessels  (Fig.  26),  and 
the  pulmonary  circulation  becomes  of  much  greater  im- 
portance than  before."  J 

The  branchial  blood  vessels,  or  aortic  arches, 
are  six  in  number,  and  lie  in  the  visceral  arches, 
the  afferent  vessel  lying  parallel  and  posterior 
to  the  efferent  vessel  (Fig.  26).  Of  the 
branchial  vessels,  only  those  lying  in  the  first, 
second,  third,  and  fourth  arches  are  func- 
tional, the  vessels  of  the  mandibular  and  hyoid 
arches  being  in  a  rudimentary  condition. 

Although  the  afferent  and  efferent  vessels 
lie  so  close  together,  there  is  at  first,  as  has 
been  said,  no  communication  between  them 
except  through  the  gill  capillaries  (Fig.  23) 
which  are  given  off  from  their  sides,  first  to 
the  external  and  then  to  the  internal  gills.  As 
the  direct  communication  between  the  afferent 
and  efferent  vessels,  which  lies  near  the  ven- 
tral end  of  the  arch  (Fig.  26),  becomes  larger 
it  is  evidently  easier  for  the  blood  to  flow 

J  Marshall. 


The  Development  of  the  Frog      63 

through  that  passage  than  to  pass  through  the 
fine  capillaries  of  the  gills,  so  that  the  supply 
of  blood  to  the  gills  is  gradually  cut  off,  and 
the  amount  of  blood  that  goes  to  the  lungs  is 
correspondingly  increased  ;  but  for  a  time  the 
tadpole  breathes  both  by  gills  and  by  lungs. 

If  the  tadpole  be  prevented  from  coming  to 
the  surface  to  breathe,  as  by  fastening  wire 
netting  just  below  the  surface  of  the  water,  it 
is  said  that  the  change  to  the  lung-breathing 
condition  may  be  indefinitely  postponed. 

The  changes  in  the  circulation  that  take 
place  at  metamorphosis  are  chiefly  concerned 
with  changes  in  the  branchial  blood  vessels, 
or,  as  they  are  called  after  the  disappearance 
of  the  capillaries  and  the  establishment  of 
the  direct  communication,  the  aortic  arches. 
Some  of  the  details  of  these  changes  have  not 
been  made  out  as  satisfactorily  as  is  to  be  de- 
sired, but  the  main  points  are  pretty  definitely 
established. 

Since  the  branchial  blood  vessels  in  the  man- 
dibular  and  hyoid  arches  are,  from  the  first, 
rudimentary,  they  may  be  disregarded  in  this 
discussion.  After  the  establishment  of  the  di- 
rect communication  between  the  afferent  and 
efferent  branchial  vessels,  the  blood  passes 


FIG.  23. 


FIG.  23.  A. — DIAGRAMMATIC  FIGURE  OF  THE  HEAD  AND  ANTE- 
RIOR PART  OF  THE  BODY  OF  A  7~MM.  TADPOLE,  SHORTLY  AFTER 
HATCHING  ;  SHOWING  THE  BRANCHIAL  BLOOD  VESSELS  FROM  THE 
VENTRAL  SURFACE.  THE  HEART  HAS  BEEN  REMOVED. 

B.— SAME  EMBRYO.  FROM  THE  RIGHT  SIDE.  THE  HEART  is  REP- 
RESENTED IN  SITU,  BUT  THE  EXTERNAL  GILLS  OF  THE  FIRST  AND 
SECOND  BRANCHIAL  ARCHES  HAVE  BEEN  CUT  OFF  SHORT  AT  THEIR 

BASES.     (After  Marshall.) 

A,  dorsal  aosta.  A  B,  basilar  artery.  A  C,  carotid  artery.  AF.\,A  F.2, 
A  F.'S,  afferent  branchial  vessels  of  the  first,  second,  and  third  branchial  arches. 
A  /*,  pulmonary  artery.  A  /?,  anterior  cerebral  artery.  A  7\  anterior  palatine 
artery.  C/4,  anterior  commissural  vessel.  CP,  posterior  commissural  vessel. 
E  F.\,  EF.2,  EF3,  E FA,  efferent  branchial  vessels  of  the  first,  second,  third, 
and  fourth  branchial  arches.  EH^  efferent  vessel  of  hyoid  arch.  E  M,  efferent 
vessel  of  mandibular  arch.  GE,  external  sills.  GM,  glornerulus.  KA^  seg- 
mental  duct.  K P,  head-kidney  or  pronephros.  K S.\,  KS.3,  first  and  third 
nephrostomes  of  head-kidney.  L  F.4,  efferent  lacunar  vessel  of  fourth  branchial 
arch.  RA,  auricle.  R  V^  ventricle.  R  T,  truncus  arteriosus.  KZ>,  Cuvierian 
vein.  V H,  hepatic  veins.  V  K,  vein  of  sucker.  V M,  mandibular  vein.  V  F, 
hyoidean  vein. 


TC 


TR 


FlG.  24. — A  I2-MM.  TADPOLE  DISSECTED  FROM  THE  VENTRAL 
SURFACE  TO  SHOW  THE  HEART,  THE  INTERNAL  GILLS,  THE  BRAN- 
CHIAL VESSELS,  AND  THE  HEAD-KIDNEYS  AND  THEIR  DUCTS.  THE 
TAIL,  WHICH  IS  ABOUT  DOUBLE  THE  LENGTH  OF  THE  HEAD  AND 

BODY,  HAS  BEEN  REMOVED.     X  22.     (After  Marshall.) 

A,  dorsal  aorta.  A  F.\,  A  F.3,  afferent  branchial  vessels  of  first  and  th'rl 
branchial  arches.  A  L,  lingual  artery.  CG,  carotid  gland.  EA,  junction  be. 
tween  afferent  and  efferent  branchial  vessels  of  first  branchial  arch.  E  F.\,  E  F3, 
efferent  branchial  vessels  of  first  and  third  branchial  arches.  GM,  glomerulus. 
KA,  archinephric  or  segmental  duct.  KM,  Wolffian  tubules.  K P,  prone- 
phros  or  head-kidney.  K  S.\^  A'6".3,  first  and  third  nephrostomes  of  head-kidney  - 
L  /,  upper  lip.  LJ,  lower  lip.  L  P,  hind  limb.  O  A ,  aperture  of  opercular 
cavity.  O  P,  opercular  cavity.  R  S,  sinus  venosus.  R  7",  truncus  arteriosus. 
R  V,  ventricle.  TC,  cloaca.  TO,  oesophagus,  cut  short.  T R,  rectal  spout. 


66 


The  Development  of  the  Frog     67 

from  the  bulbus  arteriosus  directly  around  the 
pharynx,  through  the  four  aortic  arches,  into 
the  dorsal  aorta.  Previous  to  this  time  a 
branch  has  grown  out  from  the  fourth  aortic 
arch  to  the  lung,  the  pulmonary  artery  (Fig. 

26,  AP),  and  as  the  gills  diminish  more  and 
more  in  size,  this  vessel  becomes  larger  and 
larger    until   it  carries  all    of  the   blood  that 
formerly   went    to    the   gills   for    purification. 
From  the  lungs  the  blood  is  brought  back  di- 
rectly to  the  heart  by  the  pulmonary  veins. 

The  first  aortic  arch,  on  the  completion  of 
metamorphosis,  becomes  the  carotid  arch  of 
the  frog,  which  carries  blood  to  the  head  (Fig. 

27,  i).     That   portion  of  the  dorsal   aorta  be- 
tween the   openings   of  the    first    and  second 
aortic  arches  may  remain  open,  but  more  com- 
monly becomes  entirely  obliterated. 

The  second  aortic  arch  of  the  tadpole  be- 
comes the  systemic  arch  of  the  adult  frog 
(Fig.  27,  2). 

The  third  aortic  arch  gradually  diminishes 
in  size,  and  eventually  entirely  disappears. 

The  fourth  aortic  arch  of  the  tadpole  be- 
comes the  pulmo-cutaneous  arch  of  the  frog, 
carrying  blood  to  the  lungs  and  skin,  as  the 
name  would  indicate  (Figs.  26  and  27,  3). 


68 


Vertebrate  Embryology 


It  retains  its  connection  with  the  dorsal  aorta 
for  a  considerable  time,  but  eventually  be- 
comes separated  from  it,  so  that  all  of  the 
blood  that  now  passes  from  the  bulbus  arte- 
riosus  directly  to  the  aorta  must  pass  through 
the  third  or  systemic  arch  (Fig.  27,  2). 


FIG.  25. — DIAGRAMS  TO  ILLUSTRATE  THE  MODE  OF  DEVELOP- 
MENT OF  THE  HEART. 

En^  entoderm.  EC,  ectoderm.  £,  endothelial  lining  of  the  heart. 
M,  muscular  wall  of  heart.  Mes,  mesoderm.  PC,  pericardium.  PA, 
pharynx.  (Somewhat  altered  from  Morgan.) 

The  carotid  gland,  a  characteristic  structure 
in  the  anatomy  of  the  frog,  is  formed  as  an 
elaboration  of  the  direct  communication  be- 
tween the  afferent  and  efferent  vessels  of  the 
first  branchial  arch. 

The  development  of  the  other  blood  vessels 
will  be  described  in  connection  with  the  chick, 


The  Development  of  the  Frog     69 

where  they  approach  more  nearly  the  condition 
in  man  and  other  mammals. 

The  spleen,  since  it  is  so  intimately  associated 
with  the  blood,  may  be  mentioned  at  this  time. 
"  The  spleen  arises  as  a  spherical  bud  on  the 
mesenteric  artery  :  it  consists  of  cells  similar  to 
those  of  the  lymphatic  tissue,  and,  like  these, 
is  said  to  be  derived  originally  from  the  ento- 
blast  cells  of  the  mesenteron."  1 

DEVELOPMENT  OF  THE  CCELOM  AND  THE  MUS- 
CULAR SYSTEM 

The  formation  of  the  mesoblast  as  a  layer 
of  cells  between  the  ectoblast  and  entoblast, 
and  the  splitting  of  this  mesoblast  into  two 
layers,  the  somatopleure  and  splanchnopleure, 
with  the  body-cavity  or  ccelom  between  them, 
has  already  been  mentioned  (Fig.  15). 

The  sheet  of  mesoblast  on  each  side  of  the 
body  rapidly  grows  ventralward  until  it  meets 
and  fuses  with  its  fellow  of  the  opposite  side, 
so  that  there  is  very  early  a  complete  layer 
of  mesoblast  over  the  ventral  side  of  the 
embryo  (Figs.  13,  M,  and  15).  Along  the 
mid-dorsal  line,  however,  the  two  sheets  of 
mesoblast  remain  distinct,  being  separated  by 

1  Marshall. 


70  Vertebrate  Embryology 

the  notochord  (Fig.  13,  N).  In  the  anterior 
end  of  the  embryo  the  mesoblast  is  much 
thinner,  and  does  not  there  split  into  the  two 
layers. 

On  each  side  of  the  notochord  the  meso- 
blast becomes  thickened  to  form  the  segmental 
plate,  which  does  not,  at  first,  show  any  sepa- 
ration into  two  layers  ;  later,  however,  the 
body-cavity  does  extend  into  the  segmental 
plate,  for  a  time,  but  eventually  disappears 
from  that  region. 

At  about  the  time  when  the  medullary  folds 
are  coming  together  to  form  the  neural  canal, 
the  segmental  plate  on  each  side  of  the  noto- 
chord begins  to  be  broken  up  into  blocks  by 
a  series  of  vertical  connective  tissue  septa 
at  right  angles  to  the  notochord.  These 
blocks  or  segments  are  the  mesoblastic  somites 
or  myotomes.  The  mesoblastic  somites  are,  at 
first,  not  separated  from  the  lateral  sheets  of 
mesoblast,  but  very  soon  after  their  formation 
they  become  separated  from  the  lateral  meso- 
blast, and,  by  the  thickening  of  their  walls, 
especially  the  inner,  their  cavities  are  ob- 
literated. At  a  somewhat  later  stage  the 
mesoblastic  somites  are  largely  converted  into 
muscles,  whose  >-shaped  arrangement  may  be 


The  Development  of  the  Frog      71 

easily  seen  in  the  transparent  tail  of  the  young 
tadpole  (Fig.  i ,  M-O).  The  lateral  plates  of  the 


A     GM   AB    AU      EFj    Efe    CP      EFJ 


AS 


AL 


VD    Af.+  RB 


FlG.  26. — A  DIAGRAMMATIC  FIGURE  OF  THE  HEAD  AND  NECK  OF 
A  I2-MM.  TADPOLE,  FROM  THE  RIGHT  SIDE,  TO  SHOW  THE  HEART  AND 
BRANCHIAL  VESSELS.  THE  GILLS  AND  THE  GILL  CAPILLARIES  ARE 

NOT  REPRESENTED.     X  35-     (After  Marshall.) 

A,  dorsal  aorta.  A  B,  basilar  artery.  A  F.\,  A  F.2,  A  FA,  afferent  branchial 
vessels  of  first,  second,  and  fourth  branchial  arches.  A  L,  lingual  artery.  A  P, 
pulmonary  artery.  A  R,  anterior  cerebral  artery.  A  S,  posterior  palatine  artery. 
A  71,  anterior  palatine  artery.  A  U,  cutaneous  artery.  A  V,  pharyngeal  artery. 
CA,  anterior  commissural  vessel.  CG,  carotid  gland.  CP,  posterior  commis- 
sural  vessel.  £  F.I,  E  F.2.  E  F.3,  E  FA,  efferent  branchial  vessels  of  first,  second, 
third,  and  fourth  branchial  arches.  G  M,  glomerulus.  RA,  right  auricle.  RB, 
left  auricle.  R  T,  truncus  arteriosus.  R  V,  ventricle.  V D,  Cuvierian  vein. 
V H,  hepatic  vein.  VI,  posterior  vena  cava.  V P,  pulmonary  vein. 

mesoblast,  the  somatopleure  and  the  splanch- 
nopleure,  remain   comparatively  thin  and  are 


72  Vertebrate  Embryology 

largely  converted  into  muscle,  the  somato- 
pleure  and  ectoblast  forming  the  body  wall, 
while  the  splanchnopleure  and  entoblast  form 
the  wall  of  the  digestive  tract. 

By  the  separation  of  the  somatopleure  and 
splanchnopleure  the  ccelom  is  greatly  enlarged, 
and,  at  the  same  time,  a  small  portion  is  sepa- 
rated from  the  anterior  end  as  \he  pericardial 
cavity. 

THE  DEVELOPMENT  OF  THE  SKELETON 

"The  vertebral  column. — The  earliest  skeletal  struc- 
ture, and  for  a  time  the  only  one,  is  the  notochord,  the 
development  of  which  from  the  hypoblast  of  the  mid- 
dorsal  wall  of  the  mesenteron  has  already  been  described. 
It  forms  a  cellular  rod  extending  from  the  blastopore  to 
the  pituitary  body  ;  and  as  the  tail  is  formed,  it  extends 
back  into  it.  The  notochord  consists  of  vacuolated 
cells,  filled  with  fluid,  and  is  invested  by  a  delicate 
structureless  sheath  (Figs.  12  and  13,  N}. 

"  About  the  time  of  appearance  of  the  hind  legs,  a 
delicate  skeletal  tube,  at  first  soft,  but  soon  becoming 
cartilaginous,  is  formed  round  the  notochord  from  the 
mesoblast.  This  tube  grows  upwards  at  the  sides  of 
the  spinal  cord,  as  a  pair  of  longitudinal  ridges,  with 
which  a  series  of  cartilaginous  arches,  which  appeared 
at  the  sides  of  the  spinal  cord  at  a  slightly  earlier  stage, 
very  soon  become  continuous. 

"  By  the  appearance  of  transverse  lines  of  demarcation, 
the  cartilaginous  sheath  of  the  notochord  becomes  cut 


The  Development  of  the  Frog      73 

up  into  a  series  of  nine  vertebra,  followed  by  a  posterior 
unsegmented  portion,  which  later  becomes  the  urostyle. 
This  transverse  division  does  not  affect  the  notochord, 
which  remains  as  a  continuous  structure  until  the 
complete  absorption  of  the  tail  at  the  end  of  the  met- 
amorphosis. Shortly  after  the  metamorphosis  thin  rings 


FIG.  27.— DIAGRAMMATIC  FIGURE  OF  THE  ARTERIAL  SYSTEM  OF 

THE  MALE  FROG,  FROM  THE  RIGHT  SIDE.       (After  Marshall.) 

a,  stomach.  b,  nostril.  c,  small  intestine,  c  a,  carotid  artery.  c& 
carotid  gland,  cm,  coeliaco-mesenteric  artery,  c n,  cutaneous  artery,  d,  large 
intestine,  d n,  dorsal  aorta.  /.  femur.  A,  spleen,  ha,  hepatic  artery,  i. 
right  lung,  la,  lingual  artery.  ;;/,  testis.  o,  kidney,  oa,  occipito-vertebral 
artery,  pa,  pulmonary  artery,  r,  pelvic  girdle,  j,  sternum,  sa,  subclayian 
artery,  sc,  sciatic  artery.  ^,  tongue.  ta,  truncus  arteriosus.  ua^  urino- 
genital  arteries,  v,  ventricle.  1,  carotid  arch.  2,  systemic  arch.  3,  pulmo- 
cutaneous  arch. 


of  bone,  slightly  constricted  in  their  centres,  so  as 
to  be  hourglass-shaped  in  section,  are  developed  in  the 
membrane  investing  the  cartilaginous  sheath  of  the 
notochord  :  these  correspond  with  the  nine  vertebrae 
already  present,  and  form  the  first  rudiments  of  the 
vertebral  centra.  Jn  the  intervertebral  regions,  between 
the  successive  bony  rings,  annular  thickenings  of  the 


74  Vertebrate  Embryology 

cartilaginous  sheath  occur,  which  grow  inwards  so  as  to 
constrict  and  ultimately  obliterate  the  notochord.  Each 
of  these  vertebral  rings  becomes,  after  the  metamorpho- 
sis, divided  into  an  anterior  and  a  posterior  portion, 
which  fuse  with  the  bony  centra  of  the  adjacent  verte- 
brae, and  ossify  to  form  their  articular  ends. 

"  From  the  circumference,  and  from  the  articular  ends 
of  each  vertebra,  ossification  gradually  spreads  inwards  ; 
but  a  small  portion  of  notochord  persists  in  the  middle 
of  each  centrum  for  a  long  time,  or  even  throughout 
life. 

"  The  vertebrae  are  not  placed  opposite  the  myotomes, 
but  alternate  with  these  ;  so  that  each  vertebra  is  acted 
on  by  two  myotomes  on  each  side,  one  pulling  it  for- 
wards, and  the  other  backwards. 

"  The  transverse  processes  are  at  first  independent  of 
the  corresponding  vertebrae,  but  very  early  fuse  with 
them.  They  extend  into  the  septa  between  the  myo- 
tomes, and  probably  correspond  to  the  ribs  of  other 
vertebrates. 

"  The  urostyle  is  the  part  of  the  axial  skeleton  behind 
the  vertebrae  ;  it  is  not  divided  into  vertebrae  at  any 
stage  in  development.  The  anterior  end  of  the  noto- 
chord, imbedded  in  the  base  of  the  skull,  is  gradually 
encroached  on  by  the  cartilage  and  bone  around  it,  and 
ultimately  completely  absorbed. 

"  The  skull. — The  skull  of  the  tadpole  consists  almost 
entirely  of  cartilage  ;  none  of  the  bones  of  the  skull, 
with  the  exception  of  the  parasphenoid,  appearing  until 
nearly  the  time  of  metamorphosis.  In  the  adult  frog 
this  cartilaginous  skull  is  replaced  to  a  considerable  ex- 
tent by  cartilage  bone  ;  while  other  bones,  primitively 


The  Development  of  the  Frog       75 

distinct,  and  probably  of  dermal  origin— the  membrane 
bones — graft  themselves  to  it. 

*'  The  three  morphologically  distinct  elements  of  which 
the  skull  consists  may  with  advantage  be  described  sepa- 
rately. 

"  a.  The  cranium,  or  brain  case. — This  in  its  fully 
formed  condition  is  an  unsegmented  cartilaginous  tube, 
enclosing  the  brain:  it  is  developed  as  follows  : 

"  In  the  front  part  of  the  head  a  pair  of  longitudinal 
cartilaginous  bars,  the  trabecula  cranii,  appear  in  tad- 
poles of  about  10  mm.  length:  these  grow  back  along- 
side of  the  notochord  as  a  pair  of  horizon \.z\  parachordal 
rods  (Fig.  32). 

"  The  hinder  ends  of  the  trabeculae  are  some  little 
distance  apart,  and  between  them  is  a  space  in  which 
the  pituitary  body  lies.  In  front  of  this  pituitary  fossa, 
the  trabeculse  unite  to  form  a  plate  of  cartilage,  which 
underlies  the  anterior  end  of  the  brain,  and  is  produced 
into  blunt  processes  at  its  outer  angles. 

"The  parachordals  grow  rapidly:  they  extend  in- 
wards so  as  to  meet  each  other  both  above  and  below 
the  notochord,  which  they  now  completely  surround. 
The  two  parachordals  soon  fuse  together  to  form  the 
basilar  plate,  which,  with  the  trabeculae,  forms  a  firm  car- 
tilaginous floor  to  the  brain  case.  At  their  hinder  ends 
the  parachordals  grow  upwards  to  form  the  side  walls 
of  the  cranium.  Further  forwards  the  pituitary  foramen 
becomes  closed  by  a  thin  plate  of  cartilage,  and  the  lat- 
eral margins  of  the  parachordals  and  trabeculae  grow 
upwards  so  as  to  form  the  side  walls  of  the  skull,  the 
roof  remaining  imperfect  in  this  region. 

"  The  first  bone  to  be  developed  is   the  parasphenoid. 


AF.3 


OR 


TC 


LP 


TR 


FlG.  28. — A  40-MM.  TADPOLE  DISSECTED  FROM  THE  VENTRAL 
SURFACE  TO  SHOW  THE  HEART,  THE  BRANCHIAL  VESSELS,  AND  THE 
HEAD-KIDNEYS  AND  WOLFFIAN  BODIES.  THE  TAIL  HAS  BEEN  CUT 

OFF.      X  5-     (After  Marshall.) 

A,  dorsal  aorta.  A  F.\,  A  F.3,  afferent  branchial  vessels  of  first  and  third 
branchial  arches.  A  L,  lingual  artery.  CG,  carotid  gland.  E  F.\,  E  FS,  effer- 
ent branchial  vessels  of  first  and  third  branchial  arches.  F,  fat  body.  GM, 
glomerulus.  A' A,  archinephric  or  segmental  duct.  KM,  Wolffian  bodv.  K P, 
pronephros  or  head-kidney,  now  degenerating.  LA,  fore-limb,  st;ll  within  oper- 
cular  cavity.  L  /,  upper  lip.  LJ,  lower  Up.  L  P,  hind-limb.  OR,  genital 
ridge.  R  T,  truncus  arteriosus.  R  V,  ventricle.  T C,  cloaca.  TO,  oesophagus, 
cut  short.  T  R,  cloacal  spout. 


The  Development  of  the  Frog     77 

The  exoccipitals,  the  frontals  and  parietah,  which  are 
the  first  to  separate,  and  other  bones  soon  follow;  and 
by  the  time  the  metamorphosis  is  complete  and  the 
tail  absorbed,  all  the  bones  of  the  adult  cranium  are 
present,  except  the  sphenethmoid,  which  does  not  appear 
till  some  months  later. 

"  b.  The  sense  capsules. — The  cartilaginous  auditory 
capsules  appear  in  tadpoles  of  about  12  mm.  length  as 
thin  shells  of  cartilage  investing  the  auditory  vesicles. 
They  are  at  first  quite  independent  of  the  cranium,  but 
before  the  completion  of  the  opercular  folds  they  fuse 
with  the  upgrowing  parachordals  to  form  part  of  the 
side  walls  of  the  skull.  The  pro-otic  appears  at  about 
the  time  of  completion  of  the  metamorphosis. 

"  The  optic  capsules  are  thin  shells  of  cartilage,  form- 
ing part  of  the  sclerotic  coats  of  the  eyes.  They  arise 
about  the  same  time  as  the  auditory  capsules,  and,  un- 
like the  other  sense  capsules,  they  remain  distinct  from 
the  cranium  throughout  life,  in  order  to  secure  mobility 
of  the  eyeballs. 

"  The  olfactory  capsules  are  from  their  first  appearance 
very  closely  connected  with  the  anterior  ends  of  the 
trabeculse,  which  grow  up  between  them  to  form  the 
median  vertical  internasal  septum.  They  develop  later 
than  the  auditory  and  optic  capsules."  l 

c.  The  visceral  skeleton. —  The  cartilaginous  bars 
lying  in  the  visceral  arches  make  up  what  is  known 
as  the  visceral  skeleton,  and  as  the  structure  and  fate 
of  these  bars  were  described  in  a  previous  section, 
a  more  detailed  discussion  will  be  left  until  the  similar 
structures  in  the  chick  are  taken  up. 
1  Marshall. 


78  Vertebrate  Embryology 

THE    DEVELOPMENT    OF    THE     URO-GENITAL 
ORGANS 

THE  URINARY  ORGANS 

There  are  several  points,  in  connection  with 
the  development  of  the  urinary  organs  in  the 
frog,  that  have  been  differently  described  by 
various  investigators.  We  shall  here  follow 
the  description  given  by  Marshall,  whom  we 
shall  quote  at  some  length. 

i.   General  Account 

"  The  excretory  organs  of  the  tadpole,  during  the 
early  stages  of  its  existence,  are  the  head  kidneys  or 
pronephra.  These  are  a  pair  of  globular  organs  im- 
bedded in  the  dorsal  wall  of  the  body  at  its  anterior 
end,  immediately  behind  the  constricted  neck  region 
(Figs.  24  and  28,  K P).  Each  head  kidney  is  a  con- 
voluted tube  with  glandular  walls,  opening  into  the 
body- cavity  by  three  ciliated  mouths  or  nephrostomes 
(Fig.  24,  K  S),  and  continued  back  along  the  dorsal 
wall  as  the  archinephric  or  se.gmental  duct,  K  A,  to  the 
hinder  end  of  the  body,  where  it  joins  with  the  cor- 
responding duct  of  the  opposite  side,  and  opens  into 
the  cloaca.  The  head  kidneys  and  their  ducts  are 
well  developed  in  the  tadpole  at  the  time  of  hatching: 
they  subsequently  increase  considerably  in  size,  and 
are  the  sole  excretory  organs  of  the  tadpole  during 
its  early  stages.  In  tadpoles  of  about  12  mm.  length 
the  adult  kidneys  or  Wolffian  bodies  (Fig.  24,  KM}, 


The  Development  of  the  Frog      79 

begin  to  form  in  the  hinder  part  of  the  body  as  a  series 
of  paired  tubules,  which  grow  towards  and  open  into 
the  segmental  duct.  These  Wolffian  tubules  rapidly 
increase  in  number,  as  well  as  in  size  and  complexity, 
and  become  bound  together  by  connective  tissue  to 
form  the  compact  Wolffian  bodies  or  kidneys  of  the 
fully  formed  tadpole  (Fig.  28,  KM).  At  the  same 
time  the  head  kidneys  diminish  in  size,  and  undergo 
degenerative  changes,  and  by  the  time  of  the  meta- 
morphosis (Fig  29,  K  P)  have  almost  completely  dis- 
appeared. The  Wolffian  bodies  persist  as  the  kidneys 
of  the  frog;  and  by  a  series  of  further  changes  the 
ureters  and  generative  ducts  of  the  adult  become 
established. 

2.    The  Head  Kidney  and  its  Duct 

"  In  tadpoles  of  about  3^  mm.  length,  /.  ^.,  some  time 
before  hatching,  a  pair  of  longitudinal  grooves  appears 
along  the  inner  surface  of  the  somatopleure,  extending 
from  the  neck  to  the  hinder  part  of  the  body,  and 
lying  a  little  distance  to  the  right  and  left  of  the  noto- 
chord  (Fig.  15,  K  £\  The  lips  of  each  groove  soon 
meet  and  fuse  so  as  to  convert  the  groove  into  a  tube 
or  duct.  The  closure  of  the  tube  takes  place  from 
behind  forwards,  and  at  the  anterior  end  is  effected 
imperfectly,  three  holes  or  nephrostomes,  one  behind 
another,  being  left,  through  which  the  tube  opens  into 
the  body-cavity.  As  the  embryo  grows,  the  anterior 
end  of  the  duct  becomes  convoluted  and  twisted  on 
itself  to  form  a  ball,  the  three  nephrostomes  becom- 
ing at  the  same  time  lengthened  out  into  short  tubes 
(Fig.  30).  This  convoluted  mass  is  the  head  kidney  or 


FlG.  29. — A  TAILED  FROG,  NEAR  THE  CLOSE  OF  THE  METAMOR- 
PHOSIS, DISSECTED  FROM  THE  VENTRAL  SURFACE  TO  SHOW  THE  KID- 
NEYS AND  REPRODUCTIVE  ORGANS.  X  4.  (After  Marshall.) 

A,  dorsal  aorta.  F,  fat  body.  G M,  glomerulus.  A'/4,  archinephric  or 
segmental  duct.  KM,  Wolffian  body.  K  P,  head-kidney,  disappearing.  K  £/, 
ureter.  (?,  mouth.  O R^  genital  ridge,  ^i  V^  tip  of  ventricle.  T O,  oesophagus, 
cut  short. 


80 


The  Development  of  the  Frog      81 

pronephros.  The  hinder  part  of  the  duct  is  the  archi- 
nephric  or  segmental  duct:  it  remains  straight,  or  nearly 
so,  and  shortly  before  the  tadpole  hatches  acquires  an 
opening  into  the  cloaca. 

u  At  the  time  of  hatching,  the  excretory  organs  thus 
consist  on  each  side  of  (i)  a  head  kidney,  which  is  a 
convoluted  tube  lined  by  a  glandular  epithelium,  and 
opening  into  the  anterior  end  of  the  body-cavity  by 
three  ciliated  openings,  the  nephrostomes;  and  (2)  the 
archinephric  or  segmental  duct,  which  is  the  posterior 
part  of  the  tube,  and  runs  back  along  the  dorsal  body- 
wall  nearly  straight  to  the  cloaca,  into  which  it  opens. 

"  The  head  kidney  is  closely  surrounded  by,  indeed 
almost  imbedded  in,  the  posterior  cardinal  vein  (Fig. 
31,  VC),  and  it  is  from  the  blood  of  this  vein  that  the 
epithelial  cells  of  the  head  kidney  tubules  separate  the 
excretory  matters,  which  are  then  passed  down  the  duct 
to  the  exterior. 

"  The  head  kidney  continues  to  increase  in  size,  the 
tubules  becoming  still  more  convoluted,  and  lateral  diver- 
ticula  arising  from  their  sides,  until  the  tadpole  is  about 
12  mm.  in  length,  and  the  hind  limbs  are  just  commen- 
cing to  appear.  It  remains  stationary  for  a  time  and  then, 
in  tadpoles  of  about  20  mm.  length,  begins  to  degen- 
erate; the  tubules  become  obstructed;  some  of  them  be- 
come collapsed,  others  for  a  time  irregularly  dilated; 
the  whole  organ  steadily  diminishes  in  size,  and  in  tad- 
poles of  40  mm.  (Fig.  28,  K P)  is  not  more  than  half  its 
former  size.  It  now  shrinks  rapidly,  and  at  the  time 
of  the  metamorphosis  (Fig.  29,  K P)  has  almost  dis- 
appeared, all  three  nephrostomes  having  closed  up,  and 
the  organ  being  reduced  to  a  few  small  pigmented  and 

6 


82  Vertebrate  Embryology 

irregularly  twisted  tubules,  which  have  separated  from 
the  duct,  and  which  soon  disappear  completely. 

"Opposite  the  head  kidney  an  irregular  sacculated 
outgrowth,  the  glomerulus,  arises  from  the  aorta  on  each 
side  (Figs.  28  and  31,  GM)\  this  appears  first  at  about 
the  time  of  hatching,  and  its  development  keeps  pace 
with  that  of  the  head  kidney.  It  lies  immediately  oppo- 
site the  nephrostomes,  and  very  close  to  these,  though 
not  touching  them.  It  begins  to  diminish  in  size  at 
about  the  same  time  as  the  head  kidnev.  At  the  time 


FIG.  30. — DIAGRAMS  TO  ILLUSTRATE  THE  DEVELOPMENT  OF  THE 
HEAD-KIDNEY.  (Somewhat  altered  from  Morgan.) 

of  the  metamorphosis  (Fig.  29,  GM)  it  is  very  small, 
and  after  the  first  year  it  can  no  longer  be  recognized. 
Its  close  relation  to  the  head  kidney,  and  the  fact  that 
its  growth  and  subsequent  degeneration  keep  pace  with 
those  of  the  head  kidney,  point  to  a  close  physiological 
connection  between  the  two  organs,  though  it  is  not 
easy  to  imagine  what  precise  function  the  glomerulus 
subserves. 

3.   The   Wolffian  Body 

"  The  Wolfrian  body,  or  kidney,  first  appears  in  tad- 
poles of  from  10  to  12  mm.  in  length.  It  arises  on  each 
side  as  a  series  of  small  solid  masses  of  mesoblast  cells 


The  Development  of  the  Frog      83 

lying  along  the  inner  side  of  the  segmental  duct,  between 
this  and  the  aorta  (Fig.  24,  KM}.  They  develop  from 
behind  forwards,  the  hindermost  pair  being  a  short  dis- 
tance in  front  of  the  cloaca,  and  the  most  anterior  ones 
about  three  segments  behind  the  head  kidney. 

"  These  solid  masses  soon  become  elongated  into 
twisted  rods,  which  then  become  tubular,  and  growing 
towards  the  segmental  duct  meet  and  open  into  it.  At 
their  opposite  ends  these  Wolffian  tubules,  as  they  are 
termed,  dilate  into  bulb-like  expansions,  which  become 
doubled  up  by  ingrowths  of  little  blood  vessels,  derived 
from  the  dorsal  aorta,  and  so  form  Malpighian  bodies. 
From  the  necks  of  the  Malpighian  bodies,  short  solid  rods 
of  cells  grow  towards  the  peritoneal  epithelium  and  fuse 
with  it.  These  rods  soon  become  hollow,  and  open  into 
the  body-cavity  by  ciliated  funnel-shaped  mouths  or 
nephrostomes:  their  opposite  ends  break  away  from  the 
Wolffian  tubules  and  open  directly  into  the  renal  veins 
on  the  ventral  surface  of  the  kidney.  The  Wolffian 
tubules  rapidly  increase  in  number;  they  also  branch 
freely,  and  so  give  rise  to  a  complicated  system  of  glandu- 
lar tubules,  which,  when  bound  together  by  blood  vessels 
and  connective  tissue,  form  the  Wolffian  body  or  kidney 
of  the  frog.  The  nephrostomes  persist;  and  in  the  adult 
frog  as  many  as  200  or  more  are  present  on  the  ventral 
surface  of  the  kidney,  as  minute  funnel-like  ciliated 
openings,  leading  by  short  tubes  into  the  renal  veins. 

4.  The  Wolffian  and  Miillerian  Ducts 

"  So  far  we  have  only  described  one  duct  on  each 
side,  the  segmental  duct,  which  acts  as  the  excretory 
duct  first  of  the  head  kidney,  and  then  of  the  Wolffian 


84 


Vertebrate  Embryology 


body  as  well.  We  have  now  to  consider  in  what  way  the 
ureters  and  generative  ducts  of  the  adult  frog  are  formed. 
About  the  time  of  the  metamorphosis  the  head  kidney, 


ML 


w 


FIG.  31. — TRANSVERSE  SECTION  THROUGH  THE  BODY  OF  A  TAD- 
POLE AT  THE  TIME  OF  HATCHING  ;  THE  SECTION  PASSING  THROUGH 
THE  SECOND  PAIR  OF  THE  NEPHROSTOMES,  AND  THE  THIRD  PAIR  OF 

MYOTOMES.      X  50.     (After  Marshall.) 

A,  aorta.  C,  cceolom  or  body-cavity.  Cff,  notochord.  CJ,  subnoto- 
chordal  rod.  G  M^  glomerulus.  K P,  segmental  or  archinephric  duct.  K  S, 
second  nephrostome  of  left  side.  M  £,  somatopleuric  layer  of  mesoblast.  M  //, 
splanchnopleuric  layer  of  mesoblast.  ML,  myotome.  N L,  lateral  line  branch 
of  pneumogastric  nerve.  N  S,  spinal  cord.  Z1,  intestinal  region  of  mesenteron. 
V  C,  posterior  cardinal  vein.  rat  hepatic  vein.  IV,  liver  diverticulum. 

which  has  become  rudimentary,  separates  completely 
from  the  duct,  which  now  ends  blindly  a  short  distance 
in  front  of  the  Wolffian  body. 


The  Development  of  the  Frog      85 

"A  little  later,  after  completion  of  metamorphosis  and 
the  entire  disappearance  of  the  tail,  this  anterior  end  of 
the  segmental  duct,  in  front  of  the  Wolffian  body,  be- 
comes divided  somewhat  obliquely  into  two  ;  an  anterior 
part,  which  is  now  isolated  from  the  Wolffian  body,  and 
will  be  called  the  Mullerian  duct ;  and  a  posterior  part, 
the  Wolffian  duct,  which  is  simply  the  posterior  part  of 
the  original  segmental  duct,  and  receives  the  Wolffian 
tubules  of  the  kidney. 

"  The  Mullerian  duct  becomes  connected  in  front  with 
the  peritoneal  epithelium,  and  acquires  an  opening  into 
the  anterior  end  of  the  body-cavity.  At  its  hinder  end 
it  grows  back  along  the  outer  side  of  the  Wolffian  duct 
to  the  cloaca,  into  which  it  opens.  So  far  the  changes 
are  the  same  in  both  sexes.  In  the  male  frog  the  Mul- 
lerian duct  persists  in  this  condition  throughout  life,  and 
may  be  recognized  as  a  slender,  longitudinal  streak  lying 
in  the  thickness  of  the  peritoneum  a  short  distance  to  the 
outer  side  of  the  kidney,  and  extending  some  distance  in 
front  of  it.  In  the  female  frog  the  Mullerian  duct  be- 
comes the  oviduct,  the  anterior  opening  being  carried 
forward  first  as  a  groove,  and  then  by  closure  of  the  lips 
as  a  tube,  to  the  position  characteristic  of  the  peritoneal 
opening  of  the  adult  oviduct ;  while  the  posterior  part 
becomes  greatly  convoluted  and  acquires  thick  glandular 
walls  ;  the  hindermost  part  of  the  oviduct  remains  thin- 
ner walled,  but  of  much  greater  capacity. 

"  The  Wolffian  duct  becomes  in  both  sexes  the  ureter. 
In  the  female  frog  it  undergoes  no  further  change  of 
importance.  In  the  male  frog  the  hinder  end  of  the 
Wolffian  duct  becomes  dilated  into  a  much-branched 
glandular  enlargement,  the  vesicula  seminalis. 


A  BH 


QO 


RL 


CM   BR*  BRJBR.2  BR.i 


FIG.  32.     A. — THE  SKULL  OF  A   I2-MM.  TADPOLE,  SEEN  FROM 

THE  RIGHT  SIDE.  THE  NOTOCHORD,  THE  BRAIN,  AND  THE  ENTIRE 
HEAD  ARE  REPRESENTED  IN  OUTLINE,  IN  ORDER  TO  SHOW  THE  RE- 
LATIONS OF  THE  SKULL  TO  THEM. 

B. — THE  SAME  SKULL  FROM  THE  DORSAL  SURFACE.       THE    LOWER 
JAW  AND  THE  HYOIDEAN  AND  BRANCHIAL  BARS  ARE  OMITTED. 

C. — SAME  SKULL  FROM  THE  VENTRAL  SURFACE.     (A,  B,  and  C 
are  all  from  Marshall.) 

BB,  basi-branchial.  BH,  roof  of  hind-brain.  B  M ,  roof  of  mid-brain. 
BR.\,  B  R.2,  B  /?.3,  B  RA,  first,  second,  third,  and  fourth  branchial  bars.  BS, 
cerebral  hemisphere.  CH,  notochord.  K  C,  auditory  capsule.  H  B,  basihyal. 
HO,  urohyal.  H  Q,  articulation  of  ceratohyal  with  quadrate.  H R,  ceratohyal. 
J L,  lower  jaw.  J U,  upper  jaw.  L  /,  upper  lip.  LJ,  lower  lip.  LL,  lower 
labial  cartilage.  L  U,  upper  labial  cartilage.  M  C,  Meckel's  cartilage.  PN, 
pineal  body.  Q,  quadrate.  Q  O,  orbital  process  of  quadrate.  QP.  palato-ptery- 
goid  process.  Q  /?,  connection  of  quadrate  with  trabecula.  R  C,  paracprdal 
cartilage.  R  L,  trabecula  cranii.  S A^  membranous  patch  in  which  stapes  is  de- 
veloped later.  X,  choroid  plexus  of  third  ventricle. 

86 


The  Development  of  the  Frog      87 

5.    The  Vasa  Efferentia 

"  In  both  sexes  at  an  early  stage,  as  the  Malpighian 
bodies  are  forming  in  the  Wolffian  body,  those  nearest  to 
the  genital  ridges  give  off  tubular  branches  from  their 
capsules  into  the  ridges. 

"  In  the  female  frog  these  tubules  are  said  to  expand 
very  greatly,  and  to  give  rise  to  the  chambers  or  cavities 
in  the  adult  ovary  ;  but  the  point  is  not  established  with 
certainty. 

"  In  the  male  frog  these  tubules  become  the  vasa  effer- 
entia;  they  become  connected  with  the  spermatic  tubules, 
and,  as  at  the  other  ends  they  open  into  the  Wolffian 
tubules,  they  form  passages  along  which  the  spermatozoa 
can  get  from  the  testis  to  the  Wolffian  duct  or  ureter, 
and  so  out." 

THE  GENITAL  ORGANS 

The  reproductive  organs  begin  to  develop 
in  young  tadpoles  shortly  after  the  opening  of 
the  mouth,  as  longitudinal  ridges  or  thicken- 
ings of  the  peritoneal  epithelium,  lying  near 
the  mesentery  and  close  to  the  inner  bor- 
ders of  the  kidneys.  These  thickenings  are 
known  as  the  genital  ridges,  and  are  found  in 
all  tadpoles,  there  being  as  yet  no  sexual 
distinctions. 

From  the  posterior  two  thirds  of  the  genital 
ridges  the  ovaries,  or  testes,  as  the  case  may 


88  Vertebrate  Embryology 

be,  develop,  while  from  the  anterior  third  the 
fat  bodies  are  developed. 

The  genital  ridge  is  primarily  formed  by  the 
change  in  the  shape  of  the  cells  of  the  perito- 
neal epithelium  at  that  place.  While  most  of 
the  epithelial  cells  of  the  peritoneum  are  flat, 
those  that  are  to  form  the  genital  ridge  become 
more  cuboidal  or  columnar,  at  the  same  time 
dividing  and  becoming  several  cells  deep  ;  a 
vascular  core  of  connective  tissue  now  grows 
into  the  genital  ridge  from  the  basement  mem- 
brane of  the  peritoneum. 

Some  of  these  epithelial  cells  grow  more 
rapidly  than  the  rest  and  become  spherical  in 
shape,  while  the  smaller  cells  collect  around 
the  large  ones  to  form  capsules  or  follicles. 
The  large  round  cells  are  known  as  primi- 
tive germ  cells  or  gonoblasts,  and  from  them 
are  developed,  at  the  time  of  metamorpho- 
sis, when  the  sexes  become  differentiated, 
either  true  ova  or  eggs,  in  the  case  of  the 
female,  or  spermatozoa,  in  the  case  of  the 
male. 

The  limits  of  this  work  will  not  permit  a  de- 
scription of  the  histological  changes  that  take 
place  in  the  conversion  of  the  primitive  ova 
into  the  true  sexual  elements,  and,  indeed, 


The  Development  of  the  Frog      89 

there  are  some  points  in  this  process  that  are 
not  fully  determined  with  certainty. 

The  development  of  the  oviduct,  etc.,  has 
been  sufficiently  described  in  connection  with 
the  urinary  organs. 


CHAPTER  II 

THE  DEVELOPMENT  OF  THE    CHICK 
THE  EGG 

THE  egg  of  the  chick  (Fig.  33)  is  of  large 
size,  ovoid  in  shape  and  usually  some- 
what larger  at  one  end  than  at  the 
other.  It  is  protected  by  a  more  or  less  hard 
shell  of  organic  material  impregnated  with  cal- 
careous salts.  Lying  close  to  the  inside  of  the 
shell  is  the  shell  membrane,  which  is  of  two 
layers ;  these  two  layers,  sometimes  called  the 
inner  and  outer  shell  membranes,  are  closely 
attached  to  each  other  except  at  the  large  end 
of  the  egg  where  they  are  separated  somewhat 
to  form  the  air  space  (Fig.  33,  a).  The  shell 
and  the  membranes  are  sufficiently  porous  to 
allow  gases  to  pass  through  them  slowly. 

Filling  the  space  inside  of  the  shell  mem- 
branes is  the  white  or  albumen  of  the  egg,  in 
the  centre  of  which,  in  turn,  lies  the  yolk.  At 
opposite  poles  of  the  yolk,  and  apparently 

9o 


The  Development  of  the  Chick      91 

attached  to  it,  are  the  chalaz&,  which  seem  to 
be  merely  more  condensed  portions  of  the 
albumen  that  are  twisted,  and  have  been  said 
to  serve  to  hold  the  yolk  in  the  centre  of  the 
egg,  though  it  is  difficult  to  see  how  they  can 
serve  any  such  purpose,  as  they  are  not  at- 
tached at  their  outer  ends. 

The  yolk  is  the  essential  part  of  the  egg  and 
corresponds,  as  has  been  previously  pointed 
out,  to  the  true  ovum  or  egg  of  the  frog,  or 
other  animals.  It  is  bright  yellow  in  color, 
spherical  in  shape,  and  about  an  inch  in  diam- 
eter. It  is  surrounded  and  held  in  shape  by 
the  thin,  elastic  vitelline  membrane,  and  ex- 
hibits on  one  side,  normally  the  upper  one,  no 
matter  how  the  egg  has  been  opened,  a  small, 
whitish  circle,  the  blastoderm  or  cicatricula 
(Fig.  33,  b  /).  The  yolk  substance  is  made  up 
of  a  great  number  of  yolk  granules,  of  which 
two  main  kinds  may  be  distinguished,  the  yel- 
low and  the  white.  If  the  yolk  of  a  hard-boiled 
egg  be  carefully  cut,  with  a  sharp  knife,  ver- 
tically through  the  blastoderm,  it  will  be 
noticed  that  the  white  and  the  yellow  yolk  are 
arranged  in  concentric  layers,  the  yellow  being 
the  more  abundant  ;  and  that  there  is  a  flask- 
shaped  mass  of  white  granules  in  the  centre  of 


Vertebrate  Embryology 


the  yolk   so  situated  that  the  top  of  the  neck 
of  the  flask  lies  under  the  blastoderm. 

Although  of  so  large  a  size,  the  yolk  of  the 
hen's  egg  is  a  single  cell,  its  great  size  being 
chiefly  due  to  the  large  number  of  yolk  gran- 


shm 


alb 


alb 


FIG.  33.  —  SEMI-DIAGRAMMATIC  VIEW  OF  THE  EGG  OF  THE  DO- 
MESTIC FOWL,  AT  THE  TIME  OF  LAYING.  (After  Parker  and  Hes- 
well,  slightly  altered  from  Marshall.) 

rt,  air-space.  «/£,  dense  layer  of  albumen.  alb\  more  fluid  albumen. 
£/,  blastoderm,  ch^  chalaza.  sh,  shell,  s  h.m,  shell-membrane.  sh.m.\^ 
sk.m.'Z,  its  two  layers  separated  to  enclose  air-cavity. 


ules  which  it  contains.  These  yolk  granules 
serve  as  food  for  the  developing  embryo  ;  and 
it  is  to  the  abundance  or  scarcity  of  this  food 
yolk  that  the  great  variation  in  the  sizes  of 
ova  is  largely  due.  In  mammals,  for  example, 
there  is  practically  no  food  yolk,  and  the  eggs 


The  Development  of  the  Chick      93 

are  of  almost  microscopic  size  ;  hence  the 
mammalian  embryo  is  dependent  upon  its 
mother  for  food  during  its  development,  and 
an  arrangement  known  as  ti\.e  placenta  is  pres- 
ent to  permit  an  interchange  of  food  and  gases 
between  the  blood  of  the  parent  and  that  of 
the  embryo.  The  frog's  egg,  though  so  much 
smaller  than  that  of  the  chick,  contains  a  large 
amount  of  food  material,  as  we  have  already 
seen,  and  the  embryo  frog  develops  quite  inde- 
pendently of  its  mother ;  but  while  the  chick, 
at  the  time  of  hatching,  has  practically  the 
adult  structure,  the  young  frog,  at  the  time  of 
hatching,  is  a  very  different  animal  from  the 
adult  frog,  and  must  obtain  food  for  its  further 
growth  from  its  surroundings. 

The  preceding  is  a  description  of  the  egg 
at  the  time  of  its  laying.  Such  an  egg  has 
already  passed  through  the  earlier  stages  of  its 
development,  and  is  in  a  resting  condition, 
simply  awaiting  suitable  conditions  of  tem- 
perature, moisture,  etc.,  to  proceed  with  its 
complete  development.  The  statement  that 
the  yolk  is  a  single  cell  is  really  true  only 
from  the  time  it  leaves  the  ovary  until  it  is 
fertilized,  or  until  a  short  time  after  fertiliza- 
tion, when  segmentation  begins. 


94  Vertebrate  Embryology 

MATURATION  OF  THE  EGG 
Since  the  processes  of  maturation  in  the 
chick  take  place  long  before  the  egg  is  laid,  it 
is  very  difficult  to  work  them  out,  and  they  are 
imperfectly  known :  but  it  is  probable  that  the 
changes  that  take  place  are  more  or  less  simi- 
lar to  those  that  have  been  briefly  described  in 
speaking  of  the  maturation  of  the  frog's  egg. 
The  nucleus  or  germinal  vesicle  of  the  grow- 
ing ovum  is  large,  and  lies  near  the  centre  of 
the  egg ;  but  as  the  egg  matures,  the  nucleus 
moves  towards  the  surface  and  eventually  lies 
just  beneath  the  vitelline  membrane,  in  a  len- 
ticular area,  the  germinal  disc,  which  is  nearly 
free  from  food  yolk. 

When  fully  ripe,  the  egg  bursts  from  the 
ovary  into  the  body-cavity,  and  enters  the 
funnel-like  end  of  the  oviduct.  As  it  passes 
through  the  upper  or  thin-walled  part  of  the 
oviduct,  it  has  secreted  around  it,  by  the  walls 
of  the  oviduct,  the  white  or  albuminous  en- 
velope, in  spiral  bands;  the  spiral  arrangement 
being  especially  evident  in  the  more  dense 
albumen  of  the  chalazae.  This  spiral  arrange- 
ment is  caused  by  the  rotation  of  the  ovum  by 
the  spirally  arranged  folds  in  the  upper  part  of 
the  oviduct.  It  probably  takes  about  three 


The  Development  of  the  Chick     95 

hours  for  the  egg  to  pass  through  the  upper 
part  of  the  oviduct.  The  egg  next  passes 
into  the  lower  part  of  the  oviduct,  or  uterus, 
where  it  remains  for  a  considerable  time, 
twelve  to  eighteen  hours,  and  where  it  receives 
the  shell  membranes  and  the  shell.  The  length 
of  time  which  the  egg  remains  in  the  uterus 
varies  considerably,  and  there  is  a  correspond- 
ing variation  in  the  state  of  development  when 
the  egg  is  finally  laid. 

FERTILIZATION  OF  THE  EGG 

The  same  difficulties  that  were  encountered 
in  the  study  of  the  maturation  of  the  hen's 
egg  are  met  in  the  study  of  the  processes  of 
fertilization,  since  those  processes  take  place, 
as  a  matter  of  course,  before  the  egg  enters 
the  uterus  where  the  shell  is  formed.  About 
all  that  is  known  with  certainty  is  that  the 
spermatozoon  enters  the  egg  in  the  upper  part 
of  the  oviduct,  or  even  before  it  leaves  the 
ovary,  so  that  development  has  usually  been 
taking  place  for  a  good  many  hours  before  the 
egg  is  laid. 

The  spermatozoa  are  said  to  retain  their 
power  of  impregnation  for  about  two  weeks. 


96  Vertebrate  Embryology 

SEGMENTATION  OF  THE  EGG 

Segmentation  begins  at  about  the  time  the 
egg  enters  the  uterus,  and  is  usually  completed 
when  the  egg  is  laid  ;  so  that  the  hen's  egg  is 
in  a  more  advanced  state  of  development,  at 
the  time  of  laying,  than  is  the  frog's  egg. 

It  will  be  remembered,  in  the  case  of  the 
frog,  that,  in  the  process  of  segmentation,  the 


FIG.   34.      A.  —  YOLK  WITH  THE  BLASTODERM  IN  THE 

CENTRE,  THE  LATTER  SHOWING  THE  FIRST  TWO  CLEAVAGE 
PLANES.  B. — THE  BLASTODERM,  ON  A  LARGER  SCALE  AND 
AT  A  LATER  STAGE  OF  SEGMENTATION.  THE  OUTLINES  OF  A 
DOZEN  OR  MORE  CELLS  MAY  BE  SEEN.  (After  Duval.) 

entire  egg  was  divided  by  the  segmentation 
planes  that  passed  through  it ;  but  that  the 
blastomeres  or  segments  into  which  the  egg 
was  divided  were  not  all  of  the  same  size. 
Such  a  case,  where  the  whole  egg  is  divided 
by  the  segmentation  planes,  is  known  as  com- 
plete or  holoblastic  segmentation  ;  and  where,  as 


The  Development  of  the  Chick      97 

in  this  case,  also,  the  blastomeres  are  of  unequal 
size,  the  segmentation  is  said  to  be  unequal. 
A  more  common  form  of  cleavage,  seen,  for 
example,  in  the  starfish,  is  where  the  entire 
egg  divides  into  equal  blastomeres ;  this  is 
known  as  complete  and  equal  segmentation. 
The  holoblastic  form  of  cleavage  is  common 
in  the  case  of  small  eggs  where  the  food  yolk 
is  in  small  quantity. 

In  other  eggs,  such  as  those  of  Birds,  Rep- 
tiles, and  many  Arthropods,  we  have  what  is 
known  as  meroblastic  or partial 'cleavage  ;  in  this 
form  of  segmentation  the  cleavage  planes  do  not 
extend  entirely  through  the  egg,  so  that  only 
a  part  of  the  egg  is  divided  into  the  segments 
or  blastomeres.  In  the  Arthropods  there  is  a 
superficial  layer  of  protoplasm  entirely  round 
the  egg  that  is  free  from  yolk,  and  it  is  in 
this  layer  that  segmentation  takes  place  ;  such 
a  form  of  partial  segmentation  is  known  as 
superficial, 

In  the  chick  we  have  an  example  of  what  is 
known  as  discoidal  segmentation.  Instead  of 
having,  as  in  the  Arthropods,  a  layer  of  yolk- 
free  protoplasm  entirely  round  the  egg,  there 
is,  in  the  chick,  a  small  disc-shaped  area,  the 
above-mentioned  germinal  disc,  lying  on  one 


98  Vertebrate  Embryology 

side  of  the  egg ;  and  segmentation  is  confined 
to  this  small  area.  We  have,  then,  these  four 
main  methods  of  segmentation  :  the  complete, 
which  may  be  equal  or  unequal,  and  the  par- 
tial, which  may  be  superficial  or  discoidal. 


FIG.  35. — SURFACE  VIEW  OF  THE  BLASTODERM 
AT  A  LATER  STAGE  OF  SEGMENTATION  THAN  THAT 
SHOWN  IN  FIG.  34  B.  ALSO  SOMEWHAT  MORE 
ENLARGED.  (After  Duval.) 

It  may  be  well,  at  this  point,  to  give  a  brief 
description  of  the  relation  between  the  amount 
and  distribution  of  the  food  yolk,  and  the 
phenomena  of  segmentation  and  gastrulation. 

Total  cleavage  occurs  in  eggs  which,  as  a 
rule,  are  small,  and  which  contain  a  small  or 
moderate  amount  of  yolk.  If  this  small 


The  Development  of  the  Chick      99 

amount  of  yolk  be  evenly  distributed  through- 
out the  egg,  the  cleavage  will  be  equal,  as  in 
the  eggs  of  Amphioxus  and  Mammals.  If  the 
yolk  be  rather  more  abundant,  and  be  concen- 
trated nearer  one  pole  (vegetative)  of  the  egg, 
the  cleavage  will  be  unequal  (usually  only  after 
the  third  division),  as  in  the  eggs  of  Cyclo- 
stomes  and  Amphibia. 

Partial  cleavage  takes  place  in  eggs  which 
are  often  very  large,  and  which  contain  a  large 
amount  of  yolk.  This  food  yolk  is  so  un- 
equally distributed  that  the  egg  contents  may 
be  divided  into  a  formative  yolk,  in  which 
alone  the  process  of  cleavage  takes  place,  and 
a  nutritive  yolk,  which  does  not  divide  and 
which  serves  as  food  for  the  nourishment  of  the 
growing  embryo.  If  the  food  yolk  be  accu- 
mulated at  one  pole  of  the  egg  segmentation 
will  be  confined  to  a  disc-shaped  area  of  forma- 
tive yolk  situated  at  the  opposite  or  animal 
pole ;  this  is  the  discoidal  form  of  cleavage 
found  in  Fishes,  Reptiles,  and  Birds. 

When  the  food  yolk  is  collected  at  the  centre 
of  the  egg,  with  the  formative  yolk  investing 
it,  the  cleavage  will  be  superficial.  The  nucleus 
is,  in  this  case,  usually  in  the  centre  of  the  egg, 
and  the  daughter  nuclei  which  are  formed  by 


ioo          Vertebrate  Embryology 

its  division  migrate  to  the  superficial  layer  of 
protoplasm  which  then  divides  into  as  many 
segments  as  there  are  daughter  nuclei.  In  this 
way  a  germ-membrane  is  formed  around  the 
outside  of  the  egg.  This  form  of  cleavage  is 
illustrated  by  many  Arthropods. 

At  the  close  of  segmentation  the  egg,  as 
was  described  in  connection  with  the  frog,  is 
converted  into  a  hollow  sphere  known  as  the 
blastula. 

By  a  process  of  invagination  the  blastula  is 
converted  into  a  gastrula,  a  two-walled  sac, 
opening  to  the  exterior  by  the  blastopore.  As 
the  blastula  is  the  result  of  the  process  of  seg- 
mentation, its  form  will  be  dependent  upon  the 
amount  and  distribution  of  the  food  yolk  ;  and 
in  like  manner  the  character  of  the  gastrula- 
tion  will  also  depend  upon  the  yolk. 

In  some  eggs  gastrulation  is  so  plain  and 
evident  that  it  may  easily  be  made  out,  but 
in  other  eggs  it  is  so  masked  by  the  large 
amount  of  food  yolk  that  it  is  very  difficult  to 
determine. 

Four  kinds  of  gastrulse  are  sometimes  de- 
scribed : 

i.  Where  the  egg  is  small  and  free  from 
yolk,  as  in  Amphioxus,  the  archenteron  is  wide, 


The  Development  of  the  Chick    101 

and  each  germ-layer  is  made  up  of  a  single 
layer  of  cylindrical  cells.  This  is  a  simple  and 
typical  form  of  gastrula. 

2.  In    some    forms,   the    Amphibia,   for  ex- 
ample, the  large  mass  of  yolk  is  accumulated 
on  the   floor  of  the  archenteron  and  reduces 
that  cavity  to  a  narrow  fissure. 

3.  In  Fishes,   Reptiles,  and  Birds  the  egg  is 
large  and    contains  a   large  amount   of  food 
yolk.     Since   this  yolk   does  not   segment,   it 
can  take  no  part  in  the  process  of  invagination 
which    is    confined,    in    consequence,    to    the 
germinal   disc.     The  yolk  is  very  slowly  en- 
closed by  a  cellular  wall,  the  ectoderm  grow- 
ing around  it  most  rapidly,  and  the  mesoderm 
being  the  last  to  enclose  it. 

4.  In   Mammals  the  egg  is  small,  and   the 
inner  germ-layer  is  derived  from  the  thickened 
region  of  the  blastula,  probably  by  a  process 
of  invagination,  since  an  aperture  comparable 
to  the  blastopore  of  Birds  is  seen  at  a  later 
stage.     For  a  time  the  inner  germ  layer  ends 
freely  below,  so  that  the  archenteron  is  closed 
below  by  the  ectoderm  only,  a  condition  compar- 
able to  that  found  in  Birds,  if  we  imagine  the 
yolk   material  to  have  been  absorbed  before 
the  completion  of  the  middle  germ-layer. 


102          Vertebrate  Embryology 

In  vertebrates  the  gastrula  is  distinctly  bi- 
laterally symmetrical,  so  that  the  future  head 
and  tail  ends,  as  well  as  the  dorsal  and  ventral 
sides,  of  the  embryo  may  be  recognized. 

In  the  chick,  with  which  we  are  now  espe- 
cially concerned,  we  have  seen  that  the  seg- 
mentation was  confined  to  the  small  germinal 
disc,  and  that  it  was  completed  by  the  time  the 
egg  was  laid. 

The  first  indication  of  segmentation  that  is 
seen  is  a  slight  vertical  furrow  extending  across 
the  centre  of  the  germinal  disc,  but  not  reach- 
ing quite  to  the  sides  (Fig.  34,  A).  Soon 
another  vertical  furrow  is  formed  at  right 
angles  to  the  first,  so  that  the  germinal  disc 
is  now  divided  into  four  equal  parts  (Fig. 
34,  A).  Four  radial  furrows  are  next  formed, 
lying  about  half-way  between  the  first  two, 
and  then  several  cross-furrows  divide  the  eight 
radial  segments  into  smaller  central  and  larger 
peripheral  ends  (Fig.  34,  B).  The  central 
group  of  smaller  cells  does  not  lie  exactly  in 
the  centre  of  the  germinal  disc,  but  a  little 
nearer  to  one  side  than  to  the  other  (Fig.  34). 

Furrows,  running  in  all  directions,  now 
appear  in  rapid  succession,  and  the  germinal 
disc  is  soon  divided  into  a  large  number  of 


The  Development  of  the  Chick    103 

cells  by  these  vertical  and  horizontal  cleavage 
planes.  The  cells  nearer  the  centre  of  the 
germinal  disc  continue  to  be  smaller  than 
those  nearer  the  periphery  until  nearly  the 
close  of  segmentation  (Fig  35),  when  the 
peripheral  cells  continue  to  divide  for  a  little 
longer  time  and  thus  are  finally  reduced  to 
the  same  size  as  the  central  cells.  Each  of 
these  small  cells  contains  a  nucleus  which  is 
probably  derived  from  the  repeated  division 
of  the  original  segmentation  nucleus  of  the 


THE   BLASTODERM 

By  the  time  the  egg  is  laid,  the  germinal 
disc  has  been  changed,  by  this  process  of 
segmentation,  to  a  sharply  defined  circular 
cap  of  cells  which,  by  its  less  specific  gravity, 
always  lies  at  the  upper  pole  of  the  egg,  as 
has  already  been  mentioned  (Fig.  33  bl). 
This  circular  cap  or  blastoderm  is  usually 
about  3.5  mm.  in  diameter  when  the  egg  is 
laid,  though  its  condition  at  that  time  varies 
somewhat,  depending  upon  the  length  of  time 
the  egg  remains  in  the  uterus  before  being 
laid. 

If  examined  carefully  from  the  surface,  the 


104          Vertebrate  Embryology 

blastoderm  will  exhibit  two  areas :  around 
the  periphery  of  the  disc  will  be  seen  a  band 
that  is  whiter  and  more  opaque  than  the  cen- 
tral part;  this  is  known  as  the  area  opaca; 
the  central,  more  transparent  part  is  known  as 
the  area  pellucida.  In  the  centre  of  the  area 
pellucida  may  be  seen  a  white  area  (some- 
times called  the  nucleus  of  Pander)  which  is 


ifba 


FIG.  36- — LONGITUDINAL  SECTION  OF  THE  BLASTODERM  AFTER 

THE  COMPLETION  OF  SEGMENTATION.       (After  Duval.) 

ex,  ectoderm.  /«.!,  primitive  entoderm.  bbp,  cells  that  form  the 
thickened  rim  of  the  blastoderm,  eg,  sub-germinal  cavity. 

the   top    of   the    flask-shaped    mass   of   white 
yolk  which  lies  in  the  centre  of  the  egg. 

If  vertical  sections  of  the  blastoderm  be 
made,  and  examined  under  the  microscope 
(Fig.  36),  it  will  be  found  to  be  composed 
of  two  layers  of  cells ;  the  upper  layer  or 
ectoderm  (ex)  composed  of  short  columnar 
or  cubical  cells  of  uniform  size  and  closely 
packed  together,  is  more  or  less  distinct  and 
sharply  defined  ;  the  lower  layer  of  cells  (in. i) 
is  much  less  sharply  defined  and  is  composed 


The  Development  of  the  Chick    105 

of  cells  of  various  sizes  and  shapes.  Between 
these  two  layers  is  sometimes  seen,  at  an 
early  period,  before  the  egg  is  laid,  a  very 
small  cleft-like  space,  the  segmentation  cavity, 
corresponding  to  the  large  and  distinct  cavity 
of  that  name  which  was  seen  in  the  frog's 
egg.  At  a  somewhat  later  period  may  be 
seen  a  more  distinct  cavity,  the  subgerminal 
cavity,  (eg)  lying  between  the  lower  layer  cells 
and  the  yolk. 

In  the  centre  of  the  blastoderm,  the  cells 
of  the  lower  layer  are  few  and  scattered,  while 
around  the  periphery  they  are  more  numer- 
ous and  form  a  comparatively  thick  layer 
(Fig.  36).  It  is  this  difference  in  the  thick- 
ness of  the  different  regions  of  the  blasto- 
derm that  produces  the  distinction  into  an  area 
opaca  and  an  area  pellucida,  when  the  blasto- 
derm is  viewed  from  above. 

Owing  to  the  extreme  delicacy  of  the  blasto- 
derm, it  is  difficult  to  obtain  sections  that  will 
show  the  above  points. 

During  incubation  the  blastoderm  continu- 
ally increases  in  size  until  it  completely  en- 
closes the  yolk.  In  this  growth  the  area 
opaca  increases  much  more  rapidly  than  the 
area  pellucida,  and  retains  its  circular  outline, 


io6          Vertebrate  Embryology 

while  the  area  pellucida  soon  becomes  oval  and 
then  pyriform  in  outline  (Fig.  46,  ar.  pi). 


FIG.  37.     (After  Foster  and  Balfour.) 

"Fig.  37,  A  to  N)  forms  a  series  of  purely  diagrammatic 
representations,  introduced  to  facilitate  the  comprehen- 
sion of  the  manner  in  which  the  body  of  the  embryo  is 
formed,  and  of  the  various  relations  of  the  yolk-sac, 
amnion,  and  allantois. 

"  In  all  vt  is  the  vitelline  membrane,  placed,  for  con- 
venience sake,  at  some  distance  from  its  contents,  and 
represented  as  persisting  in  the  later  stages;  in  the  actual 
egg  it  is  in  direct  contact  with  the  blastoderm  (or  yolk), 


The  Development  of  the  Chick    107 

and  early  ceases  to  have  a  separate  existence.  In  all  e 
indicates  the  embryo,  pp  the  general  pleuroperitoneal 
space,  af  the  folds  of  the  amnion  proper;  ae  or  ac  the 
cavity  holding  the  liquor  amnii;  al  the  allantois;  a'  the 
alimentary  canal;  y  or ys  the  yolk  or  yolk-sac. 

"A,  which  may  be  considered  as  a  vertical  section  taken 
longitudinally  along  the  axis  of  the  embryo,  represents 
the  relations  of  the  parts  of  the  egg  at  the  time  of  the 
first  appearance  of  the  head-fold,  seen  on  the  right-hand 
side  of  the  blastoderm  e.  The  blastoderm  is  spreading 
both  behind  (to  the  left  hand  in  the  figure),  and  in  front  (to 
the  right  hand)  of  the  head-fold,  its  limits  being  indicated 
by  the  shading  and  thickening  for  a  certain  distance  of 
the  margin  of  the  yolk  y.  As  yet  there  is  no  fold  on  the 
left  side  of  e  corresponding  to  the  head-fold  on  the  right. 

"B  is  a  vertical  transverse  section  of  the  same  period 
drawn  for  convenience  sake  on  a  larger  scale  (it  should 
have  been  made  flatter  and  less  curved).  It  shews  that 
the  blastoderm  (vertically  shaded)  is  extending  later- 
ally as  well  as  fore  and  aft,  in  fact,  in  all  directions;  but 
there  are  no  lateral  folds,  and  therefore  no  lateral  limits 
to  the  body  of  the  embryo  as  distinguished  from  the 
blastoderm. 

"  Incidentally  it  shews  the  formation  of  the  medullary 
groove  by  the  rising  up  of  the  laminae  dorsales.  Be- 
neath the  section  of  the  groove  is  seen  the  rudiment 
of  the  notochord.  On  either  side  a  line  indicates  the 
cleavage  of  the  mesoblast  just  commencing. 

**  In  C,  which  represents  a  vertical  longitudinal  section 
of  later  date,  both  head-fold  (on  the  right)  and  tail-fold 
(on  the  left)  have  advanced  considerably.  The  alimen- 
tary canal  is  therefore  closed  in,  both  in  front  and  be- 


io8  Vertebrate  Embryology 

hind,  but  is  in  the  middle  still  widely  open  to  the  yolk  y 
below.  Though  the  axial  parts  of  the  embryo  have  be- 
come thickened  by  growth,  the  body-walls  are  still  thin; 
in  them,  however,  is  seen  the  cleavage  of  the  mesoblast, 
and  the  divergence  of  the  somatopleure  and  splanch- 
nopleure.  The  splanchnopleure  both  at  the  head  and 
at  the  tail  is  folded  in  to  a  greater  extent  than  the  so- 
matopleure, and  forms  the  still  wide  splanchnic  stalk. 
At  the  end  of  the  stalk,  which  is  as  yet  short,  it  bends 
outwards  again  and  spreads  over  the  surface  of  the  yolk. 
The  somatopleure,  folded  in  less  than  the  splanch- 
nopleure to  form  the  wider  somatic  stalk,  sooner  bends 
round  and  runs  outwards  again.  At  a  little  distance 
from  both  the  head  and  the  tail  it  is  raised  up  into  a 
fold,  af,  af,  that  in  front  of  the  head  being  the  highest. 
These  are  the  amniotic  folds.  Descending  from  either 
fold,  it  speedily  joins  the  splanchnopleure  again,  and  the 
two,  once  more  united  into  an  uncleft  membrane,  extend 
some  way  downwards  over  the  yolk,  the  limit  or  outer 
margin  of  the  opaque  area  not  being  shewn.  All  the 
space  between  the  somatopleure  and  the  splanchnopleure, 
//,  is  shaded  with  dots.  Close  to  the  body  this  space 
may  be  called  the  pleuroperitoneal  cavity;  but  outside 
the  body  it  runs  up  into  either  amniotic  fold,  and  also 
extends  some  little  way  over  the  yolk. 

"Z>  represents  the  tail  end  at  about  the  same  stage  on  a 
more  enlarged  scale,  in  order  to  illustrate  the  position  of 
the  allantois  al  (which  was  for  the  sake  of  simplicity 
omitted  in  C),  shewn  as  a  bud  from  the  splanchnopleure, 
stretching  downwards  into  the  pleuroperitoneal  cavity//. 
The  dotted  area  representing  as  before  the  whole  space 
between  the  splanchnopleure  and  the  somatopleure,  it  is 


The  Development  of  the  Chick    109 


evident  that  a  way  is  open  for  the  allantois  to  extend 
from  its  present  position  into  the  space  between  the  two 
limbs  of  the  amniotic  fold  of. 


!      H 


FIG.  37. 


"£,  also  a  longitudinal  section,  represents  a  stage  still 
farther  advanced.  Both  splanchnic  and  somatic  stalks 
are  much  narrowed,  especially  the  former,  the  cavity  of 


no          Vertebrate  Embryology 

the  alimentary  canal  being  now  connected  with  the 
cavity  of  the  yolk-sack  by  a  mere  canal.  The  folds  of 
the  amnion  are  spreading  over  the  top  of  the  embryo  and 
nearly  meet.  Each  fold  consists  of  two  walls  or  limbs, 
the  space  between  which  (dotted)  is  as  before  merely  a 
part  of  the  space  between  the  somatopleure  and  splanch- 
nopleure.  Between  these  arched  amniotic  folds  and  the 
body  of  the  embryo  is  a  space  not  as  yet  entirely  closed  in. 

"F  represents  on  a  different  scale  a  transverse  section 
of  E  taken  through  the  middle  of  the  splanchnic  stalk. 
The  dark  ring  in  the  body  of  the  embryo  shews  the  posi- 
tion of  the  neural  canal,  below  which  is  a  black  spot, 
marking  the  notochord.  On  either  side  of  the  notochord 
the  divergence  of  somatopleure  and  splanchnopleure  is 
obvious.  The  splanchnopleure,  more  or  less  thickened, 
is  somewhat  bent  in  towards  the  middle  line,  but  the  two 
sides  do  not  unite,  the  alimentary  canal  being  as  yet 
open  below  at  this  spot;  after  converging  somewhat  they 
diverge  again  and  run  outwards  over  the  yolk.  The 
somatopleure,  folded  in  to  some  extent  to  form  the  body- 
walls,  soon  bends  outwards  again,  and  is  almost  immedi- 
ately raised  up  into  the  lateral  folds  of  the  amnion  of. 
The  continuity  of  the  pleuroperitoneal  cavity  within  the 
body  with  the  interior  of  the  amniotic  fold  outside  the 
body  is  evident;  both  cavities  are  dotted. 

"G,  which  corresponds  to  D  at  a  later  stage,  is  intro- 
duced to  shew  the  manner  in  which  the  allantois,  now  a 
distinctly  hollow  body,  whose  cavity  is  continuous  with 
that  of  the  alimentary  canal,  becomes  directed  towards 
the  amniotic  fold. 

"  In  H  a  longitudinal,  and  /  a  transverse  section  of 
later  date,  great  changes  have  taken  place.  The  several 


The  Development  of  the  Chick    1 1 1 

folds  of  the  amnion  have  met  and  coalesced  above  the 
body  of  the  embryo.  The  inner  limbs  of  the  several 
folds  have  united  into  a  single  membrane  (a),  which  en- 
closes a  space  (ae  or  ac)  round  the  embryo.  This  mem- 
brane (a)  is  the  amnion  proper,  and  the  cavity  within  it, 
/".  e.t  between  it  and  the  embryo,  is  the  cavity  of  the 
amnion  containing  the  liquor  amnii.  The  allantois  is 
omitted  for  the  sake  of  simplicity. 

"  It  will  be  seen  that  the  amnion  a  now  forms  in  every 
direction  the  termination  of  the  somatopelure;  the  per- 
ipheral portions  of  the  somatopleure,  the  united  outer  or 
descending  limbs  of  the  folds  of  in  (7,  Z>,  F,  G  having 
been  cut  adrift,  and  nov  forming  an  independent  con- 
tinuous membrane,  the  serous  membrane^  immediately 
underneath  the  vitelline  membrane. 

"  In  /the  splanchnopleure  is  seen  converging  to  com- 
plete the  closure  of  the  alimentary  canal  a'  even  at  the 
stalk  (elsewhere  the  canal  has  of  course  long  been  closed 
in),  and  then  spreading  outwards  as  before  over  the 
yolk.  The  point  at  which  it  unites  with  the  somato- 
pleure, marking  the  extreme  limit  of  the  cleavage  of  the 
mesoblast,  is  now  much  nearer  the  lower  pole  of  the 
diminished  yolk. 

"  As  a  result  of  these  several  changes,  a  great  increase 
in  the  dotted  space  has  taken  place.  It  is  now  possible 
to  pass  from  the  actual  peritoneal  cavity  within  the 
body,  on  the  one  hand  round  a  great  portion  of  the  cir- 
cumference of  the  yolk,  and  on  the  other  hand  above 
the  amnion  «,  in  the  space  between  it  and  the  serous 
envelope. 

"  Into  this  space  the  allantois  is  seen  spreading  in  K 
at  al. 


ii2  Vertebrate  Embryology 

"  In  L  the  splanchnopleure  has  completely  invested  the 
yolk-sac,  but  at  the  lower  pole  of  the  yolk  is  still  con- 
tinuous with  that  peripheral  remnant  of  the  somatopleure 
now  called  the  serous  membrane.  In  other  words,  the 
cleavage  of  the  mesoblast  has  been  carried  all  round  the 
yolk  (ys)  except  just  at  the  lower  pole. 


"  In  J/the  cleavage  has  been  carried  through  the  pole 
itself;  the  peripheral  portion  of  the  splanchnopleure 
forms  a  complete  investment  of  the  yolk,  quite  uncon- 
nected with  the  peripheral  portion  of  the  somatopleure, 
which  now  exists  as  a  continuous  membrane  lining  the 
interior  of  the  shell.  The  yolk-sac  (ys)  is  therefore 
quite  loose  in  the  pleuroperitoneal  cavity,  being  con- 


The  Development  of  the  Chick    113 

nected  only  with  the  alimentary  canal  («')  by  a  solid 
pedicle. 

"  Lastly,  in  JV  the  yolk-sac  (ys)  is  shewn  being  with- 
drawn into  the  cavity  of  the  body  of  the  embryo.  The 
allantois  is  as  before,  for  the  sake  of  simplicity,  omitted; 
its  pedicle  would  of  course  lie  by  the  side  of  ys  in  the 
somatic  stalk  marked  by  the  usual  dotted  shading. 

<4  It  may  be  repeated  that  the  above  are  diagrams,  the 
various  spaces  being  shewn  distended,  whereas  in  many 
of  them  in  the  actual  egg  the  walls  have  collapsed,  and 
are  in  near  juxtaposition." 

We  have  now  described,  in  some  detail,  the 
condition  of  the  egg  at  the  time  of  laying, 
and  the  changes  that  it  has  undergone  previ- 
ous to  that  time. 

To  facilitate  the  study  of  the  subject  in  the 
laboratory,  the  development  of  the  chick  from 
this  point  will  be  described  by  periods.  For 
example,  the  changes  that  take  place  during 
the  first  day  will  first  be  described,  then  all 
the  changes  of  the  second  day,  then  of  the 
third  day,  and  so  on  to  the  end  of  incubation, 
at  the  twenty-first  day.  Since  the  changes 
that  take  place  after  the  first  week  are  chiefly 
those  of  growth,  most  of  the  space  will  be 
given  to  the  changes  of  the  first  four  or  five  days. 

Before  beginning  the  more  detailed  descrip- 
tion of  the  changes  that  take  place  during 


ii4          Vertebrate  Embryology 

the  first  day,  it  may  be  well  to  give  a  very 
brief  summary  of  the  whole  process  of  de- 
velopment. 

SUMMARY  OF  DEVELOPMENT 

A  very  careful  study  of  the  series  of  dia- 
grams in  Figs.  37  and  38  will  greatly  aid  in  the 
comprehension  of  the  more  detailed  descrip- 
tion that  is  to  follow,  keeping  in  mind  that  the 
dotted  areas  marked  "  pp,"  in  Fig.  37,  are,  in 
reality,  spaces  and  not  tissue,  as  might  naturally 
be  inferred  from  the  diagrams. 

After  having  followed  the  development  of 
the  various  organs  and  systems  of  organs  in 
the  frog,  the  only  features  in  the  development 
of  the  chick  that  will  be  apt  to  give  trouble  are 
the  folding  off  of  the  embryo  from  the  yolk 
and  the  development  of  the  amnion  and  al- 
lantois,  structures  not  found  in  the  frog. 

An  understanding  of  the  way  in  which  the 
embryo  becomes  folded  off  from  the  rest  of 
the  egg  may,  perhaps,  be  obtained  in  the  fol- 
lowing way :  cut  out  four  circles  of  cloth,  say 
75  cm.  in  diameter,  of  three  different  colors. 
Put  the  two  circles  that  are  of  the  same  color 
together  and  then  put  these  two  circles  between 
the  other  two. 


The  Development  of  the  Chick    1 1 5 

Let  these  superimposed  circles  represent  a 
greatly  enlarged  blastoderm  that  has  been  re- 
moved from  the  yolk  to  which  it  was  originally 
attached.  The  upper  layer  of  cloth  will  repre- 
sent the  ectoblast,  the  bottom  layer  will  rep- 
resent the  entoblast,  and  the  two  similarly 
colored  layers  in  the  middle  will  represent  the 
two  layers  of  the  mesoblast  after  their  separa- 
tion. The  method  of  the  formation  of  these 
three  germ  layers,  during  the  first  day  of  incu- 
bation, will  be  described  under  the  head  of  the 
first  day's  development. 

As  the  yolk  takes  no  actual  part  in  the  forma- 
tion of  the  embryo,  other  than  as  a  supply  of 
food  for  the  growth  of  the  constantly  enlarging 
chick,  it  may  be  omitted  in  our  model. 

Now  spread  the  cloth  blastoderm  upon  a 
table  and  place  under  its  centre  a  small  object, 
such  as  a  bottle.  If  now  the  fingers  of  one 
hand  be  pushed  under  one  end  of  the  bottle, 
carrying,  of  course,  the  three  germ  layers  with 
them,  we  shall  have  represented  the  formation 
of  the  head  fold  that  is  represented  and  de- 
scribed in  Figs.  37  and  38.  By  pushing  under 
the  cloth  at  the  other  end  of  the  bottle,  in  the 
same  way,  we  may  represent  the  formation  of 
the  tail  fold  ;  and  in  a  like  manner  the  lateral 


n6          Vertebrate  Embryology 

folds  may  be  formed.  If  these  folds,  the  head, 
tail,  and  lateral,  be  pushed  under  far  enough 
they  will  meet  under  the  centre  of  the  bottle, 
and  we  shall  have  the  bottle,  with  its  surround- 
ing layers  of  cloth,  connected  with  the  rest  of 
the  model  by  only  a  sort  of  stalk,  which  is 
hollow  and  is  composed  of  the  three  layers  of 
cloth  (cf.  Fig.  37,  H  and  L).  The  bottle  is 
used  simply  to  give  a  solid  object  around  which 
the  folding  may  more  easily  be  done,  but  we 
are  to  consider  the  space  occupied  by  the  bottle 
as  an  empty  space. 

We  have  now  represented  what  is  sometimes 
called  the  embryo-sac,  or  simply  the  embryo,  in 
contradistinction  to  ti\£.  yolk-sac,  or  simply  the 
yolk.  The  embryo  remains  connected  with 
the  yolk  throughout  the  period  of  incubation 
by  the  yolk-  or  somatic-stalk,  and  as  the  embryo 
increases  in  size,  the  yolk-sac  is,  by  absorption, 
constantly  diminished  (Fig.  37).  The  space 
occupied  by  the  bottle,  in  our  model,  repre- 
sents the  digestive  tract  of  the  chick,  and  is 
lined,  as  will  be  seen  by  examination  of  the 
model,  by  the  lower  germ  layer  or  entoblast. 
The  body-cavity  would  be  difficult  to  represent 
in  the  cloth  model,  but  it  can  be  imagined  to 
exist  as  the  narrow  space  between  the  two 


The  Development  of  the  Chick    1 1 7 

layers  of  similarly  colored  cloth  which  we  have 
called  the  mesoblast. 

The  formation  of  the  amnion  (Fig.  38,  am./) 
may  be  represented  in  our  model  by  lifting 
up  with  the  fingers  a  small  fold  of  the  upper 


nch 


FIG.  38.  A  B — DIAGRAMS  ILLUSTRATING  THE  DEVELOPMENT  OF 
THE  FCETAL  MEMBRANES  OF  A  BIRD.     (After  Parker  and  Haswell.) 

A,  early  stage  in  the  formation  of  the  amnion,  sagittal  section.     B,  slightly 
later  stage,  transverse  section. 

and  second  layers  of  cloth,  and  pulling  these 
two  layers  back  over  the  head  end  of  the  em- 
bryo ;  this  fold  will  correspond  to  the  head-fold 
of  the  amnion  (Fig.  38,  am./).  Similar  folds 
might  be  lifted  up  at  the  posterior  end  and  at 
the  sides  of  the  embryo  model,  to  represent 


n8          Vertebrate  Embryology 

the  tail  and  lateral  folds  of  the  amnion.     The 
way  in  which  these  folds  fuse  together  will  be 


co  el 


br 


Vim 


FIG.  38.  C  D — DIAGRAMS  ILLUSTRATING  THE  DEVELOPMENT  OF 
THE  FOZTAL  MEMBRANES  OF  A  BIRD.  (After  Parker  and  Haswell.) 

C,  stage  with  completed  amnion  and  commencing  allantois.  D,  stage  in  which 
the  allantois  has  begun  to  envelop  the  embryo  and  yolk-sac.  The  ectoderm  and 
entoderm  are  represented  by  black  lines ;  the  mesoderm  is  gray. 

all,  allantois.  all',  the  same  growing  round  the  embryo  and  yolk-sac. 
am,  amnion.  am.f,  amf,  amniotic  fold,  an,  anus,  br,  brain.  coel, 
ccelome.  coel',  extra-embryonic  ccelome.  h  t,  heart,  ms.ent,  mesenteron. 
mth,  mouth,  nch,  notochord.  sp.cd,  spinal  chord,  sr.m,  serous  membrane. 
u  tnb.d,  umbilical  duct,  vt.m,  vitelline  membrane,  y  k,  yolk-sac. 

explained  later,  and  will  readily  be  understood 
by  study  of  Figs.  37  and  38. 

The  formation  of  the  allantois  cannot  readily 


The  Development  of  the  Chick    119 

be  represented  in  the  cloth  model,  but  is  easily 
understood  from  Fig.  38.  It  arises,  as  will  be 
explained  later,  as  a  thin-walled  pouch  from 
the  posterior  end  of  the  digestive  tract,  and  as 
it  increases  in  size  it  extends  up  around  the 
upper  side  of  the  embryo,  between  the  inner 
and  outer  layers  of  the  amnion  (Fig.  38,  a  //). 
Neither  the  amnion  nor  the  allantois  form 
any  permanent  part  of  the  actual  embryo,  and 
both  are  cast  off  at  the  time  of  hatching. 


CHAPTER  III 

THE  DEVELOPMENT  OF  THE   FIRST  DAY 

IN  speaking  of  the  age  or  state  of  develop- 
ment of  an  embryo,  it  is  customary  to 
date  from  the  time  of  the  beginning  of 
the  process  of  incubation,  whether  that  pro- 
cess be  carried  out  under  a  hen  or  in  an  incu- 
bator :  but  it  must  not  be  supposed  that  all 
eggs  will  reach  exactly  the  same  state  of  de- 
velopment at  the  same  time.  Various  things 
will  influence  this  state  ;  for  example,  the  season 
of  the  year,  the  length  of  time  the  egg  was 
retained  in  the  uterus  before  being  laid,  etc.; 
so  that  when  we  speak  of  an  egg  being 
at  the  thirty-six-hour  stage,  we  shall  mean 
that  the  egg  in  question  has  reached  a  state 
of  development  that  is  commonly  reached 
by  eggs  after  that  period  of  normal  incuba- 
tion. It  is  simply  a  convenient  and  com- 
monly used  method  of  speaking  of  embryos 
that  have  reached  a  certain  state  of  devel- 
opment. 

120 


Development  of  the  First  Day     121 

It  will  be  remembered  that  the  blastoderm, 
at  the  time  of  laying,  is  a  small,  disc-shaped 
structure,  like  an  inverted  watch-glass,  lying 
on  top  of  the  egg  just  beneath  the  vitelline 
membrane. 

In  sections  it  shows  two  more  or  less  dis- 
tinct layers,  the  ectoblast,  consisting  of  a  single 


FIG.  39. — PART  OF  A  SECTION  THROUGH 
THE  BLASTODERM  AFTER  THE  FORMATION  OF 
THE  DEFINITE  ENTODERM  OR  HYPOBLAST. 
(After  Duval.) 

ex,  ectoderm.     /'»,  entoderm.     m s,  mesoderm. 

layer  of  closely  packed,  columnar  cells  :  and 
the  lower  layer  cells,  which  are  more  irregular 
in  outline  and  are  not  arranged  in  so  defin- 
ite a  layer  as  are  the  cells  of  the  ectoblast 

(Fig.  36). 

One  of  the  first  changes  that  take  place, 
during  the  first  part  of  the  first  day,  is  the  for- 
mation of  a  definite  cntoblast  by  the  flattening 


122          Vertebrate  Embryology 

and  joining  together,  in  a  distinct  membrane, 
of  these  lower  layer  cells  (Fig.  39).  In 
this  process  of  the  formation  of  the  ento- 
blast,  some  of  the  lower  layer  cells  are  left 
between  the  ectoblast  and  the  newly  formed 


FIG.  40. — SURFACE  VIEW  OF  THE  EMBRYO 
AT  ABOUT  THE  SIXTEENTH  HOUR  OF  INCUBA- 
TION. (After  Duval.) 

m  f,  mesoblast  forming  the  darker  area  in  the  pos- 
terior region  of  the  area  pellucida.  X,  primitive  streak. 


entoblast ;  these  scattered  cells  probably  form, 
as  will  be  noted  later,  a  part  of  the  mesoblast 
or  middle  germ  layer.  They  are  mostly  con- 
fined to  the  posterior  end  of  the  area  pellu- 
cida, where  they  form  a  slight  opacity,  which 
is  sometimes  called  the  embryonic  shield. 


Development  of  the  First  Day     123 

The  differentiation  of  the  entoblast  begins 
in  the  centre  of  the  area  pellucida,  and  gradu- 
ally extends  towards  the  area  opaca,  where 
it  is  formed  at  a  somewhat  later  period,  and 
where  it  is  composed  of  cells  of  a  different 
shape  from  those  of  the  pellucid  area. 

While  the  entoblast  is  being  formed,  the 
blastoderm  has  increased  considerably  in  size, 
and  the  area  pellucida,  which  in  the  unincu- 
bated  egg  is  often  very  indistinct,  becomes 
sharply  marked  off  from  the  opaque  area. 

About  the  middle,  or  during  the  second 
half,  of  the  first  day,  a  very  characteristic 
structure,  the  primitive  streak,  makes  its  ap- 
pearance. With  the  naked  eye,  or  under  a  low 
power  of  the  microscope,  it  is  seen  (Fig.  40,  X) 
as  a  distinct  linear  opacity  in  the  posterior  half 
of  the  now  pear-shaped  area  pellucida. 

It  might  here  be  mentioned  that  the  broad 
end  of  the  area  pellucida  corresponds  to  the 
head  end  of  the  future  chick  ;  and  that  if 
the  egg  be  held  with  its  large  end  towards 
the  right,  in  nearly  every  case  the  head  of  the 
embryo  will  point  away  from  the  observer. 

If  vertical  sections  be  cut  through  the  primi- 
tive streak,  at  right  angles  to  its  long  axis 
(Fig.  41,  pp),  it  will  be  found  that  the  streak 


124          Vertebrate  Embryology 

is  caused  by  an  elongated  group  of  cells  that 
have  been  proliferated  off  from  the  ectoblast, 
and  now  lie  between  the  ectoblast  and  ento- 
blast.  These  cells  gradually  spread  out  on  each 
side  of  the  primitive  streak,  and  form  a  part 
of  the  mesoblastic  layer. 

The  primitive  streak,  for  a  time,  keeps  pace 


BEV    ms 


FIG.  41. — MEDIAN  PORTION  OF  A  TRANSVERSE  SEC- 
TION OF  AN  EMBRYO  AT  THE  TIME  OF  THE  FORMATION 
OF  THE  PRIMITIVE  STREAK.  (After  Duval.) 

eg',    subgerminal    cavity.      exy    ectoderm.      /«,    entoderm. 
tns,  mesoderm.    pp,  primitive  groove. 

in  growth  with  the  area  pellucida,  and  as  that 
area  grows  more  rapidly  at  its  posterior  end, 
the  primitive  streak  increases  in  length  almost 
entirely  from  its  hinder  end. 

A  median  furrow,  varying  somewhat  in 
width  and  depth,  in  different  embryos,  makes 
its  appearance  in  the  upper  surface  of  the 
primitive  streak  (Figs.  40  and  4i//),  and  is 
known  as  the  primitive  groove. 


Development  of  the  First  Day     125 

The  meaning  of  the  primitive  streak  and 
groove  has  been  much  discussed.  It  is  now 
generally  considered  to  correspond,  in  part 
at  least,  to  the  elongated  lips  of  the  blasto- 
pore  in  the  frog,  that  have  come  together, 
on  the  closure  of  the  blastopore,  as  has  been 
described  in  a  previous  part  of  this  book. 
The  primitive  groove  would  correspond  to 
the  line  of  fusion  of  the  two  lips  of  the 
blastopore. 

The  mesoblast  in  the  chick  seems  to  be 
derived  from  three  distinct  sources,  though 
it  is  not  easy  to  make  out  these  points. 

One  of  these  sources  has  been  mentioned 
in  the  primitive  streak.  A  second  source  is 
the  scattered  group  of  cells  that  was  left 
between  the  ectoblast  and  entoblast  on  the 
formation  of  the  latter  as  a  distinct  layer  of 
cells.  In  the  middle  and  lateral  parts  of  the 
area  pellucida,  at  about  the  time  of  the  form- 
ation of  the  primitive  streak,  cells  are  budded 
off  from  the  upper  side  of  the  entoblast  and 
become  mesoblast. 

The  mesoblast  cells,  derived  from  these 
three  sources,  very  soon  unite  to  form  a  con- 
tinuous layer,  so  that  it  is  impossible  to  tell 
from  which  source  any  particular  cell  was 


If] 


Development  of  the  First  Day     127 

derived  ;  this  sheet  of  mesoblast  extends  until 
it  passes  the  boundaries  of  the  area  pellu- 
cida,  and  forms  a  middle  layer  in  the  inner 
zone  of  the  area  opaca.  This  zone  of  the 
area  opaca  which  contains  the  mesoblast,  and 
which  immediately  surrounds  the  area  pellu- 
cida,  is  known  as  the  vascular  area,  because 
it  is  in  it  that  the  blood  vessels  that  absorb 
the  yolk,  for  the  growth  of  the  embryo,  are 
formed  (Fig.  80,  ar.  vase). 

The  cells  of  the  mesoblast  are  usually  not 
closely  packed  together,  and  may  generally 
be  recognized  by  their  angular  or  stellate 
form  (Figs.  42  and  48). 

At  about  the  time  of  the  formation  of  the 
primitive  streak  and  the  differentiation  of 
the  mesoblast,  the  entoblast,  in  front  of  the 
primitive  streak,  becomes  thickened  to  form 
a  longitudinal  axis  or  rod  of  cells,  the  noto- 
chord  (Fig.  42,  ch).  The  notochord  remains 
for  some  time  attached  to  the  entoblast  from 
which  it  is  derived,  but  it  later  separates 
from  this,  and  forms  a  distinct  and  separate 
rod,  similar  to  that  which  we  have  already 
seen  in  the  frog. 

While  the  entoblast  has  been  forming 
(about  the  fifteenth  to  the  twentieth  hour)  the 


FIG.  43. — THREE  TRANSVERSE  SECTIONS  ACROSS  THE  CAUDAL 
END  OF  THE  MEDULLARY  GROOVE  OF  A  CHICK  EMBRYO  WITH  SEVEN 
SEGMENTS.  (After  Minot  ) 

A,  section  through  one  of  the  segments.  B,  section  posterior  to  the  segments. 
C,  section  just  in  front  of  the  primitive  streak.  MJ.gr,  medullary  groove;  nch, 
notochord;  EC,  ectoderm;  mes,  mesoderm;  En,  entoderm  ;  Seg.  mesoblastic 
somite. 


128 


Development  of  the  First  Day     129 

ectoblast  has  become  thickened,  in  a  line  above 
the  developing  notochord,  to  form  the  medul- 
lary plate.  The  sides  of  the  medullary  plate 


St 


FIG.   44. — SURFACE  VIEW  OF  EMBRYO  AT  THE  TWENTY-THIRD 
HOUR  OF  INCUBATION.     (After  Duval.) 

A ,  anterior  limit  of  head.  /*/,  primitive  streak.  ^z>,  mesoblastic  somites. 
St,  sinus  terminalis,  bounding  the  vascular  area,  i,  region  where  the  medullary 
folds  have  almost  met  to  form  the  medullary  canal. 

soon  become  elevated  as  the  medullary  folds^ 
with  the  mediillary  groove  between  them  (Figs. 
43  and  44).  The  medullary  folds,  before  the 


130          Vertebrate  Embryology 

end  of  the  first  day,  become  very  pronounced, 
and  in  the  region  of  the  future  brain  (the 
medullary  folds,  as  was  described  in  connec- 
tion with  the  frog,  are  the  beginning  of  the 
nervous  system)  they  arch  over  until  they 
meet  in  the  middle  line  to  enclose  the  medul- 
lary canal,  though  they  do  not  actually  fuse 
together  until  a  somewhat  later  period.  The 
appearance  of  the  medullary  folds  at  the  end 
of  the  first  day  of  incubation,  as  seen  from 
the  surface,  is  shown  in  Fig.  44  (A).  It  will  be 
noticed  in  this  figure  that,  while  the  folds  are 
nearly  in  contact  for  a  considerable  part  of 
their  length,  they  are  still  widely  separated 
at  the  extreme  anterior  end,  where  a  tri- 
angular space  is  left :  and  at  the  posterior 
end  the  two  folds  diverge  widely,  and  grad- 
ually diminish  in  height  as  they  pass  back 
on  each  side  of  the  primitive  streak.  At  the 
extreme  anterior  end  the  two  folds  are  con- 
tinuous with  each  other,  across  the  base  of 
the  triangle  mentioned  above. 

During  the  second  half  of  the  first  day  the 
head-fold  makes  its  appearance,  and,  by  the 
end  of  the  day,  it  has  progressed  so  far  (Fig. 
44,  A),  that  the  head  region  of  the  embryo 
is  distinctly  marked  off.  The  formation  of 


Development  of  the  First  Day     131 

the  head-fold  has  been  illustrated  with  the 
cloth  model,  and  is  shown  in  Figs.  37  and  38: 
it  is  best  seen  in  sagittal  sections,  one  of 
which  is  represented  in  Fig  45. 


FIG.  44  (A). — ANTERIOR  PART  OF  THE  PRECEDING  FIGURE, 

MORE  HIGHLY  MAGNIFIED  TO  SHOW  DETAILS.       (After  Duval.) 

Ay  anterior  end  of  head.  C/i,  notochord.  i,  region  where  the  medullary 
folds  will  first  fuse  to  form  the  medullary  canal.  2,  lateral  limits  of  medul- 
lary folds.  3  and  4,  posterior  regions  of  medullary  folds.  5,  lateral  limits 
of  head  region.  6,  limit  of  entoderm. 

By  the  formation  of  the  head-fold  the  an- 
terior end  of  the  digestive  tract,  or  fore-gut, 
is  also  formed  (Fig.  45,  Pit).  The  tail-fold 
and  the  lateral  folds  do  not  begin  to  form 
until  later. 

In  some  cases,  before  the  end  of  the  first 


i32  Vertebrate  Embryology 

day,  a  slight  crescentic  fold  is  seen  in  the 
area  pellucida  just  in  front  of  the  head-fold 
(Fig.  44,  A)  ;  this  is  the  beginning  of  the 
amnion,  but  a  description  of  its  development, 
in  addition  to  what  has  already  been  given, 
will  be  given  at  a  later  place. 

One  of  the  most  important  changes  of  the 
latter  part  of  the  first  day  has  to  do  with  the 
mesoblast.  After  it  has  become  fully  estab- 
lished, the  mesoblast  on  each  side  of  the 
notochord  forms  (as  seen  in  cross  section) 
a  sort  of  wedge-shaped  sheet  of  tissue,  with 
the  base  of  the  wedge  next  to  the  notochord. 
At  about  the  twenty-first  hour,  each  of  these 
sheets  of  mesoblast  splits  into  two  layers 
(similar  to  the  cleavage  of  the  mesoblast  seen 
in  the  frog),  the  upper  layer  being  known  as 
the  somatopleure,  the  lower  layer  the  splanch- 
nopleure.  The  space  between  the  two  layers 
forming,  as  in  the  frog,  the  body-cavity  or 
coelom.  The  somatic  layer  becomes  closely 
associated  with  the  ectoblast  and  forms  the 
body-wall  ;  while  the  splanchnic  layer,  to- 
gether with  the  entoblast,  forms  the  wall  of 
the  digestive  tract  (Fig.  52). 

At  about  the  twenty-second  hour,  almost  im- 
mediately after  its  cleavage,  the  mesoblast  on 


-227 


7,50 


FIG.  45. — SAGITTAL  (MEDIAN  -  LONGITUDINAL)   SECTION    OF    AN 
EMBRYO  OF  26  HOURS.     (After  Duval.) 

A,  anterior  end  of  head.  CM,  medullary  canal.  EC,  endothelium  of  heart. 
RE,  limit  of  head-fold,  ex,  ectoderm,  in,  entoderm.  PC,  pericardium.  /%, 
pharynx  or  fore-gut.  Vi,  fore-brain,  b,  mesoderm. 


133 


134          Vertebrate  Embryology 

each  side  of  the  body  becomes  split  by  a  series 
of  vertical  clefts,  at  right  angles  to  the  long 
axis  of  the  body,  and  extending  for  a  short 
distance  outwards  from  the  notochord.  Im- 
mediately after  the  formation  of  these  short, 
transverse  clefts,  there  is  formed  a  vertical, 
longitudinal  cleft  on  each  side  of  the  noto- 
chord, which  divides  each  sheet  of  mesoblast 
into  a  vertebral  plate,  lying  next  to  the  noto- 
chord, and  a  lateral  plate,  lying  further  from 
the  median  line. 

The  lateral  plate  consists  of  two  continuous 
sheets  of  mesoblast,  the  somatopleure  and 
splanchnopleure ;  while  the  vertebral  plate  is 
divided  by  the  transverse  clefts  into  a  series 
of  more  or  less  cubical  blocks,  the  mesoblastic 
somites  or  proto-vertebrcz  (Figs.  44,  p  v,  and  52, 
Seg.).  The  first  pair  of  somites  is  formed  in  the 
neck  region,  and  by  the  end  of  the  first  day, 
there  are  usually  five  or  six  pairs  present.  The 
second  and  possibly  the  third  pairs  of  somites 
are  formed  in  front  of  the  first  pair ;  and  the 
others,  which  appear  in  rapid  succession,  are 
formed  in  regular  order  behind  these  first  two 
or  three  pairs. 

The  number  of  pairs  of  somites  at  any  given 
time  affords  a  convenient  method  of  estima- 


Development  of  the  First  Day     135 

ting  the  age  of  chick  embryos,  during  the  first 
two  days.  As  has  been  said,  the  first  somite 
is  formed  at  about  the  twenty-first  or  twenty- 
second  hour ;  and  at  the  end  of  the  first  day 
five  or  six  pairs  are  present.  By  the  thirty- 
sixth  hour,  there  are  about  fifteen  pairs  of 
somites  :  and  by  the  end  of  the  second  day, 
there  are  twenty-seven  or  twenty-eight  pairs. 
After  the  end  of  the  second  day  the  number 
of  somites  can  no  longer  be  used  to  esti- 
mate the  age  of  embryos,  though  the  somites 
continue  to  increase  in  number  until  the 
fourth  day.  The  somites  are  formed  in  the 
neck,  trunk  and  tail  regions,  but  do  not  ex- 
tend into  the  head. 

In  the  first  three  or  four  somites,  the  cleav- 
age of  the  mesoblast  extends  close  up  to  the 
notochord  before  the  lateral  plate  is  separated 
from  the  vertebral,  so  that  there  is  a  cavity 
in  these  somites  that  is  continuous  with  the 
body-cavity.  This  cavity  is  not  seen  in  the 
other  somites,  and  eventually  disappears  from 
these. 

The  neurenteric  canal,  which  was  described, 
in  connection  with  the  frog  (page  34),  as  a  nar- 
row passage  connecting  the  neural  canal  with 
the  extreme  posterior  end  of  the  digestive 


136          Vertebrate  Embryology 

tract,  is  seen  in  the  early  stages  of  the  chick 
embryo  as  two  or  three  small  depressions 
in  the  floor  of  the  posterior  end  of  the  neu- 
ral canal.  These  depressions  usually  appear, 
one  after  the  other,  during  the  first  three  days, 
and,  though  they  seldom  are  seen  to  open 


FIG.  46. — DIAGRAMMATIC  REPRESENTATIONS  OF  CHICK  EMBRYOS; 
A,  AFTER  TWENTY  HOURS'  INCUBATION;  B,  AFTER  TWENTY-FOUR 
HOURS'  INCUBATION.  (After  Parker  and  Haswell,  from  Marshall.) 

ar.op,  area  opaca;  ar.pl,  area  pellucida;  hd,  head;  tned.gr,  medullary 
groove;  mes,  mesoderm  indicated  by  dotted  outline  and  deeper  shade;  pr.am,  pro- 
amnion;  pr.st,  primitive  streak;  pr.  v,  proto-vertebrae. 

into  the  digestive  tract,  they  seem  to  be  homo- 
logous with  the  neurenteric  canal  of  the  frog 
and  of  other  animals. 

We  shall  now  briefly  summarize  the  more  im- 
portant changes  that  take  place  during  the 
first  day  : 

i.   The  entoblast  is  formed  by  the  rearrange- 


Development  of  the  First  Day     137 

ment  of  the  lower  layer  cells  into  a  thin  but 
definite  layer. 

2  The  primitive  streak,  with  the  primitive 
groove  along  its  axis,  is  formed  as  a  linear 
proliferation  of  cells  from  the  lower  side  of  the 
ectoblast.  These  cells  spread  out  on  each  side 
to  form  a  part  of  the  mesoblast. 

3.  The  pellucid  area  becomes  pear-shaped  ; 
and  the  vascular  area  becomes  distinguishable 
as  an  inner  zone  of  the  area  opaca. 

4.  The  medullary  plate   is  formed  in   front 
of  the  primitive  streak,  and  its  edges  become 
elevated,   as  the   medullary    folds,    and  meet 
(without  yet  fusing),  in  the  region  of  the  brain, 
to  form  the  medullary  canal. 

5.  The  notochord  is    formed  as  a  medial, 
rod-shaped    thickening    of    the    entoblast,    in 
front  of  the  primitive  streak. 

6.  The  development  of  the  head-fold  marks 
the  beginning  of  the  head. 

7.  The  mesoblast   becomes   split    into  two 
layers,  the  somatopleure   and   the   splanchno- 
pleure,  with  the  body-cavity  between  them. 

8.  The  vertebral  plates  are  separated  from 
the  lateral  plates,  and  in  the  former  about  five 
pairs  of  mesoblastic  somites  are  formed. 

It  may  be  well,  before   taking  up   the   de- 


138  Vertebrate  Embryology 

velopment  of  the  second  day,  to  emphasize 
the  importance  of  clearly  understanding  the 
changes  of  the  first  day,  and  the  changes  that 
were  described  in  the  brief  summary.  If  the 
figures  to  which  reference  is  made  are  carefully 
studied,  there  should  be  but  little  difficulty 
in  understanding  the  processes  that  are  de- 
scribed. 


CHAPTER  IV 
THE  DEVELOPMENT   OF   THE   SECOND    DAY 

IT  will  be  convenient,  and  will  facilitate  the 
study  of  sections,    in    the    laboratory,  to 
divide    the    second    day  into    two   parts  ; 
describing   first    the  changes  that   take  place 
from  the  twenty-fourth  to  the  thirty-sixth  hour, 
and   then   those   that   take   place  during  the 
second  half  of  the  day. 

FROM  THE  24TH  TO  THE  36TH    HOUR 

During  this  period  the  embryo  not  only 
becomes  much  more  clearly  outlined,  but  its 
texture  becomes  more  firm,  so  that,  while  it 
was  very  difficult  to  remove  an  eighteen-hour 
embryo  from  the  egg  without  tearing,  it  is 
quite  an  easy  matter  to  remove  an  embryo 
of  thirty  to  thirty-six  hours. 

The  medullary  folds  are  rapidly  coming 
together,  and,  by  the  thirty-sixth  hour,  the 
entire  anterior  region  is  closed  in  to  form  the 

139 


PV 


FIG.  47. — SURFACE  VIEW  (DORSAL)  OF  AN  EMBRYO  OF  33  HOURS. 
(After  Duval.) 

A  m,  head-fold  of  amnion.  C,  heart.  G  jV,  nerve  ganglion.  L  M,  medul- 
lary fold.  LP,  mesoblast  that  will  segment  into  mesoblastic  somites.  P  P,  primi- 
tive streak.  P  V,  mesoblastic  somites.  Sfi,  sinus  rhomboidalis.  V2  and  F3, 
mid-  and  hind-brains.  V A^  auditory  pits.  VO M,  vitelline  vein. 

140 


Development  of  the  Second  Day    141 

medullary  canal,  except  for  a  small  chink  at 
the  extreme  end. 

The  anterior  end  of  the  medullary  canal 
now  begins  to  enlarge  slightly  and  to  be  con- 
stricted off  from  the  rest  of  the  tube  (Fig. 
47)  this  enlargement  is  the  beginning  of  the 
fore-brain,  and  from  each  side  of  it  there 
is  soon  seen  a  small  lateral  diverticulum,  the 
optic  vesicle,  whose  further  development  will 
be  described  later. 

Behind  the  fore-brain  two  other  slight  con- 
strictions of  the  neural  canal  are  formed  (Fig. 
47)  marking  the  positions  of  the  mid-brain, 
V  2,  and  the  hind-brain,  V  3.  At  the  pos- 
terior end  of  the  embryo  the  medullary  folds 
are  still  some  distance  apart,  forming  what 
is  known  as  the  sinus  rhomboidalis  (Fig.  47, 
^  R),  along  the  floor  of  which  may  sometimes 
be  seen  the  primitive  streak,  pp. 

The  beginning  of  the  ears  may  be  seen  as 
a  pair  of  small  depressions,  the  aiiditory  pits, 
just  back  of  the  hind-brain  (Fig.  47,  V A). 

The  mesoblastic  somites  have  increased  in 
number,  and  by  the  thirty-sixth  hour,  as  has 
already  been  mentioned,  there  are  usually 
fifteen  pairs  of  them  (Fig.  47,  P  V). 

The  head  is  now  more  clearly  defined,  owing 


Vertebrate  Embryology 


partly  to  the  slight  increase  in  the  depth  of 
the  head-fold  and  partly  to  the  slight  lifting 
of  the  head  above  the  surrounding  blasto- 
derm. The  increase  in  depth  of  the  head- 
fold  causes  a  corresponding  increase  in  the 


T.C 


mes 


FJG.  48. — TRANSVERSE  SECTION  OF  A  CHICK  EMBRYO  WITH  SEVEN 
SEGMENTS;  TO  SHOW  THE  BEGINNING  OF  THE  FORMATION  OF  THE 
HEART.  (After  Minot.) 

Md,  medullary  groove;  EC,  ectoderm;  mes,  mesenchyma;  Am.  ves,  amnio- 
cardiac  vesicle;  Pk,  pharynx;  mstk,  mesothelium;  Endo^  cells  to  form  the  rudi- 
ment of  the  endothelial  heart. 


length  of  the  fore-gut  (Fig.  50),  which,  in 
cross  section  (Fig.  48,  PK),  is  a  shallow  cavity, 
in  a  dorso-ventral  direction  ;  but  is  broad  and 
crescentic,  from  side  to  side,  with  the  convex 
-side  of  the  crescent  downwards. 


Development  of  the  Second  Day    143 

THE  HEART 

During  the  first  half  of  this  day  the  heart 
makes  its  appearance  as  a  sort  of  hollow- 
ing out  of  the  mesoblast  in  the  anterior  end 
of  the  embryo,  under  the  fore-gut  (Fig.  48, 
Endd).  The  walls  of  the  heart  consist  of  an 
outer  muscular  coat,  formed  of  the  splanchnic 
mesoblast,  and  an  endothelial  lining  whose 
origin  is  said,  by  some,  to  be  from  the 
entoblast. 

The  heart  consists,  at  first,  of  two  longi- 
tudinal vessels,  in  contact  anteriorly  but  di- 
verging posteriorly,  which  together  form  a 
V-shaped  structure,  with  the  point  of  the  V 
towards  the  head  of  the  embryo. 

As  development  proceeds,  the  arms  of  the 
V  fuse  together,  from  before  back,  thus  con- 
verting the  V  into  a  Y,  with  the  stem  of  the 
Y  towards  the  head.  The  cavities  of  the  two 
tubes  that  thus  build  up  the  heart  are  at  first 
quite  distinct,  even  after  the  two  tubes  have 
come  in  contact  with  each  other :  but  they 
soon  unite  to  form  one  cavity,  the  endothelial 
lining  remaining  as  two  distinct  cavities  for 
a  short  time  after  the  muscular  walls  have 
fused.  The  muscular  walls  of  the  tubes  are 
incomplete  on  the  dorsal  side,  for  a  time, 


144          Vertebrate  Embryology 

but  after  the  fusion  of  the  tubes  the  walls  are 
completed. 

The  stem  of  the  Y,  developed  as  above 
described,  forms  the  heart  (Fig.  49,  C),  while 
the  diverging  arms  of  the  Y  are  continuous 
with  the  large  vitelline  veins  which  bring  the 
blood  back  to  the  heart  from  the  vascular 
area  (Fig.  49,  VOM). 

At  the  thirtieth  hour,  then,  the  heart  is 
a  short,  straight  tube  which  is  attached  to  the 
ventral  wall  of  the  fore-gut  or  pharynx. 

The  point  of  divergence  of  the  vitelline 
veins  is  at  the  hindermost  angle  of  the  head- 
fold,  and  as  the  head-fold  is  pushed  farther 
and  farther  back,  the  heart,  or  straight  part 
of  the  Y,  is  correspondingly  lengthened.  But 
the  tubular  heart  seems  to  grow  more  rapidly 
than  does  the  place  to  which  it  attached,  with 
the  result  that  it  is  bent  into  a  loop,  with  the 
convexity  of  the  loop  to  the  right  side  of 
the  embryo  (Fig.  49,  C).  This  looping  of  the 
heart  is  made  possible  by  the  fact  that,  while 
it  was  at  first  attached  to  the  wall  of  the  fore- 
gut  throughout  its  whole  length,  it  soon  be- 
comes detached  from  that  wall  for  the  greater 
part  of  its  length,  retaining  its  attachment 
only  at  the  ends.  The  end  of  the  heart  into 


Development  of  the  Second  Day    145 

which  the  vitelline  veins  empty  may  be  called 
the  venous,  and  the  opposite,  the  arterial 
end. 

Shortly  after  its  appearance  the  heart  begins 
to  beat  slowly,  the  pulsations  starting  at  the 
venous  and  passing  to  the  arterial  end.  This 
pulsation  of  the  heart  begins  before  there  is 
any  differentiation  of  its  mesoblast  into  mus- 
cular tissue. 

VASCULAR  SYSTEM 

The  anterior  end  of  the  heart,  which  may  be 
called  the  bulbus  arteriosus,  branches  immedi- 
ately into  two  narrow  vessels,  or  aortic  arches, 
one  of  which  passes  upwards  on  each  -side  of 
the  digestive  tract  to  its  dorsal  side,  where 
it  turns  sharply  towards  the  posterior  again  as 
the  dorsal  aorta.  The  two  dorsal  aortae  lie 
close  on  each  side  of  the  notochord  and  under 
the  mesoblastic  somites  (Fig.  54,  Ao).  At 
this  stage  of  development  they  remain  entirely 
separate  from  each  other  and  pass  back,  in  the 
position  mentioned,  towards  the  tail.  Before 
reaching  the  tail,  however,  each  gives  off  a 
large  branch,  the  branch,  in  fact,  being  larger 
than  the  aorta,  from  which  it  arises,  known  as 
the  vitelline  artery:  these  vitelline  arteries 


146          Vertebrate  Embryology 

carry  the  blood  back  to  the  vascular  area, 
whence  it  was  brought,  it  will  be  remembered, 
by  the  vitelline  veins. 

The  details  in  the  development  of  the  blood 
and  the  blood  vessels  have  been  differently 
described  by  different  workers. 


FIG.  49.  —  VENTRAL  VIEW  OF  THE  ANTERIOR  REGION  OF  THE  EM- 
BRYO SHOWN  IN  FIG.  47.     (After  Duval.) 

A0,  bulbus  arteriosus.     C,  heart,  curved  towards  the  right  side  of  the  embryo. 
/*«,  lateral  limit  of  the  cavity  of  the  pharynx.     f1,  fore-brain.     Vo,  optic  vesicle. 


^  vitelline  vein. 


According  to  one  view,  the  entire  vascular 
system  is  derived  from  mesoblast  ;  according 
to  another  view,  the  endothelial  lining  of  the 


Development  of  the  Second  Day    147 

veins  and  arteries  and  the  entire  wall  of  the 
capillaries  are  derived  from  the  entoblast. 

The  first  indication  of  the  formation  of  the 
blood  vessels  is  seen,  on  the  first  day,  as  a 
reticulated  appearance  in  that  part  of  the  meso- 
blast  surrounding  the  chick  that  has  been 
called  the  vascular  area.  This  network  be- 
comes more  distinct  during  the  second  day, 
and  begins  to  show  irregular,  reddish  blotches, 
which  are  known  as  blood  islands,  because  from 
their  cells  the  blood  corpuscles  are  formed. 
These  changes  take  place  in  the  splanchnic 
layer  of  mesoblast,  which  is  separated,  at  this 
time,  from  the  somatic  layer  by  the  extension 
of  the  body-cavity  into  the  extra-embryonic 
area  of  the  mesoblast. 

The  network  is  due  to  the  development  of 
what  is  known  as  the  angioblast,  which  is  a  set 
of  cells  collected  between  the  mesoblast  proper 
and  the  endoderm.  The  cords  of  the  angio- 
blast are  at  first  solid,  but  they  soon  acquire 
lumena,  which,  by  becoming  united,  form  a 
continuous  though  indefinite  vessel.  The  first 
of  these  channels  to  take  on  a  definite  form 
and  position  is  one  that  forms  a  sort  of  circu- 
lar boundary  to  the  entire  vascular  area  and  is 
known  as  the  sinus  terminalis  (Fig.  56).  This 


148          Vertebrate  Embryology 

indefinite  network  of  blood  vessels  lies  all  in 
one  plane,  and  the  meshes  are  more  or  less 
filled  with  mesoblast  cells. 

The  blood  islands,  which  appear  first  in  the 
area  opaca  but  soon  are  found  also  in  the  area 
pellucida,  are  spots  where  there  are  collections 
of  cells  attached  to  the  walls  of  the  blood  ves- 
sels. The  development  of  haemoglobin  in 
these  cells  gives  the  reddish  color  that  makes 
the  blood  islands  so  conspicuous  in  surface 
views  of  fresh  specimens.  The  development 
of  the  blood  islands  is  more  marked  around 
the  caudal  end  of  the  embryo. 

Soon  after  the  blood  vessels  have  become 
hollow,  the  blood  islands,  which  in  cross  sec- 
tion appear  as  local  thickenings  usually  of  the 
dorsal  walls  of  the  vessels,  bud  off  cells  into 
the  cavity  of  the  blood  vessels ;  these  cells 
form  the  first  blood  corpuscles.  It  is  from 
these  primitive  corpuscles,  according  to  a 
commonly  accepted  hypothesis,  that  all  of  the 
colored  corpuscles  of  the  body  are  descended. 
They  are  at  first  characterized  by  the  posses- 
sion of  a  rounded  nucleus,  with  a  distinct  nucle- 
olus  and  a  very  small  amount  of  protoplasm. 
After  being  set  free  in  the  lumen  of  the  blood 
vessel  the  protoplasm  of  each  cell  increases, 


Development  of  the  Second  Day    149 

and  the  cells  soon  begin  to  multiply  rapidly  by 
mitotic  division. 

The  origin  of  the  first  white  corpuscles  is 
still  uncertain.  In  the  chick  they  do  not  ap- 
pear until  about  the  eighth  day ;  and  it  seems 
probable  that  they  have  no  real  relationship  to 
the  red  corpuscles.  It  is  probable  that  they 
are  of  several  kinds  and  have  several  distinct 
origins. 

By  the  development  of  buds  from  the  ves- 
sels already  formed  the  vascular  area  continues 
to  increase  in  extent.  Some  of  these  buds, 
during  the  second  day,  begin  to  grow  towards 
and  into  the  embryo,  through  whose  tissue  they 
work  their  way  along  certain  prescribed  paths. 
While  this  growth  is  going  on,  certain  of  the 
vessels  increase  in  size  and  become  arteries  or 
veins,  while  other  vessels  remain  small  as  capil- 
laries. Certain  of  these  larger  vessels  unite 
with  the  posterior  end  of  the  heart,  which  has 
already  been  formed  and  has  begun  to  beat ; 
and  other  vessels  unite  with  the  anterior  end 
to  form  the  larger  vessels  of  the  arterial  system. 
Since  the  heart  has  begun  to  beat,  and  the 
corpuscles  have  already  been  formed,  the  cir- 
culation is  established  as  soon  as  the  blood 
vessels  become  connected  with  the  heart. 


FIG.  50. — SAGITTAL  SECTION  OF  THE  EMBRYO  REPRESENTED  IN 
FlG.  47.  (After  Duval.) 

Am,  head-fold  of  the  amnion.  A 0,  aorta.  Ch,  notochord.  CM,  medullary 
canal,  ex,  ectoderm,  i «2  entoderm.  Ph,  pharynx  or  fore-gut.  PV,  mesoblastic 
somites.  RE,  posterior  limit  of  ectoderm  of  head-fold.  IS1  and  K2,  fore-  and 
mid-brains.  VOM,  venous  portion  of  heart. 


150 


Development  of  the  Second  Day    151 

The  other  embryonic  vessels,  at  least  their 
endothelial  lining,  are  formed  by  buds  given 
off  from  these  first-formed  vessels,  just  as  hap- 
pened in  the  case  of  the  vessels  of  the  vascular 
area. 

The  outer  coats  (media  and  adventitia)  of 
the  veins  and  arteries  are  formed  by  differentia- 
tion of  the  surrounding  mesoblast. 

THE  WOLFFIAN   DUCT 

The  first  indication  of  the  uro-genital  system 
in  the  chick,  as  in  the  frog,  is  the  Wolffian 
duct. 

It  arises  at  this  time,  when  the  embryo  has 
about  ten  mesoblastic  somites,  as  a  small  ridge 
from  the  uncleft  mesoblast  that  lies  at  the 
outer  side  of  the  last  three  somites.  A  cross 
section  through  this  region  of  the  embryo  (Figs. 
52  and  54)  shows  the  Wolffian  duct  project- 
ing, on  each  side,  into  the  triangular  space 
between  the  ectoblast  above,  the  somite  on  the 
inside,  and  the  somatic  mesoblast  on  the  out- 
side. At  this  time  it  is  merely  a  solid  rod  of 
cells,  extending  for  two  or  three  somites,  and 
without  a  central  lumen. 

Summary  — The  most  important  changes  of 
the  first  half  of  the  second  day  are  : 


152  Vertebrate  Embryology 

1.  The     fusion     of     the     medullary     folds 
throughout  the  greater  part  of  their  length  to 
form  the  neural  canal. 

2.  The  dilation  of  the  anterior  end  of  the 
neural  canal  to  form  the  fore-brain,  which,  in 


Iff.C. 


F.So. 


FIG.  50  (A).  —  DIAGRAMMATIC  REPRESENTATION  OF  FIG.  50. 
(After  Foster  and  Balfour.) 

N.C.)  neural  canal.  Ch.^  notochord.  Z>,  commencing  fore-gut  or  front  part  of 
the  alimentary  canal.  F.  So,  somatopleure,  raised  up  in  its  peripheral  portion  into 
the  amniotic  fold,  Am.  Sp.,  splanchnopleure  ;  at  Sp.  it  forms  the  under  wall  of  the 
fore-gut ;  at  F.  Sp.  it  is  turning  round  to  run  forward;  just  at  its  turning-point, 
the  heart,  ///,  is  being  developed,  pp,  pleuroperitoneal  or  body  cavity.  A,  ecto- 
derm. B,  mesoderm.  C,  entoderm. 

turn,  begins  to  push  out  on  each  side  a  hollow 
diverticulum,  the  optic  vesicle  ;  and  the  indica- 
tion of  the  position  of  the  mid-  and  hind-brain 
as  slight  enlargements  of  the  neural  canal  be- 
hind the  fore-brain. 

3.  The    increase   of  the  head-fold,  and  the 
elevation   of  the  head  above  the  level  of  the 
blastoderm. 

4.  The  increase  in  the  number  of  the  mes- 
oblastic  somites. 


FIG.  51.—  SAGITTAL  SECTION  OF  AN  EMBRYO  CHICK  OF  82  HOURS. 
(After  Duval.) 


B,  spinal  canal,     BP,   lung.     C1, 
-fold. 


A/,  allantois.     Ant,   amnion.     Ao,   aorta. 

bulbus  arteriosus.  C2,  ventricle.  C3,  auricle.  Cam,  bottom  of  head-fold.  Ch, 
notochord.  CM,  wall  of  neural  tube,  CV  ,  cerebellum.  GP,  pineal  gland.  HP, 
hypophysis.  IA,  posterior  end  of  fore-gut.  IP,,  hind-eut.  MA,  rudiment  of 
wing.  Ma,  mesoblast  of  allantois.  PC,  pericardium.  Fh,  pharynx.  PP,  body 
cavity.  V1,  V*,  and  If3,  fore-,  mid-,  and  hind-brain.  VB,  liver.  VH,  cerebral 
hemisphere.  VJ,  umbilical  wall.  VOM,  vitelline  vein.  JTJT,  place  of  interruption 
of  section,  part  of  the  dorsal  region  being  omitted. 


153 


J54          Vertebrate  Embryology 

5.  The  formation  of  the  tubular  heart  and 
of  some  of  the  blood  vessels. 

6.  The  appearance  of  the  Wolffian  duct,  or, 
rather  of  a  longitudinal  rod  of  cells  that  will 
later  become  hollow  to  form  the  duct. 

FROM    THE    36TH    TO    THE    48™    HOURS. 

During  the  second  half  of  the  second  day 
the  separation  of  the  embryo  from  the  yolk-sac 
becomes  much  more  plainly  marked.  This  is 
brought  about  by  the  formation  of  a  tail-fold, 
similar  to  the  head-fold,  and  of  lateral  folds 
(Fig.  38),  so  that  by  the  end  of  this  period,  the 
whole  outline  is  distinct,  from  head  to  tail. 

The  brain.— During  this  period  the  neural 
canal  becomes  entirely  closed,  even  the  sinus 
rhomboidalis  being  fused.  The  constrictions 
that  mark  off  the  anterior  end  of  the  neural 
canal  into  what  we  have  called  the  fore-,  mid-, 
and  hind-brain  become  more  evident,  and  be- 
fore the  close  of  the  day  the  fore-brain  begins 
to  grow  forwards  as  an  unpaired  vesicle  which  is 
the  first  indication  of  the  cerebral  hemispheres. 
The  walls  of  the  brain  lie  close  under  the  ecto- 
blast,  but  between  the  two  is  seen,  in  sections, 
a  small  amount  of  mesoblast  which  will  form 
the  skull. 


Development  of  the  Second  Day    155 

The  optic  vesicles  become  considerably  elon- 
gated and  are  constricted  at  their  bases  into 
stalks.  Instead  of  projecting  straight  out 
from  the  sides  of  the  fore-brain,  they  are  now 
pressed  downwards  and  backwards. 

The  cranial  nerves  make  their  appearance 
at  the  end  of  this  period,  but  their  develop- 
ment will  be  described  later  on. 

Owing,  probably,  to  the  more  rapid  growth 
of  the  dorsal  wall  of  the  medullary  canal,  in 
the  region  of  the  mid-brain,  the  brain  becomes 
bent  downwards,  around  the  anterior  end  of 
the  notochord,  at  the  end  of  this  period,  just 
as  it  did  in  the  frog  (page  36)  :  this  downward 
bending  of  the  brain  is  known  as  cranial  flex- 
ure (Fig.  51). 

The  notochord,  whose  origin  during  the  first 
day  has  been  described,  is  by  this  time  a  con- 
spicuous cylindrical  rod,  lying  under  the  medul- 
lary canal  for  the  greater  part  of  its  length 

(Fig.  54). 

The  heart,  by  the  end  of  this  period,  has 
become  still  more  markedly  bent  and  twisted, 
so  that  it  is  now  somewhat  S-shaped,  with  the 
venous  end  rather  above  and  behind  the  arterial 
end.  The  venous  and  arterial  ends  have  ap- 
parently come  close  together,  with  the  inter- 


156          Vertebrate  Embryology 

mediate  portion  hanging  as  a  loop  between 
them.  The  venous  portion  now  forms  a  swell- 
ing on  each  side,  the  rudiments  of  the  auricles, 
while  the  arterial  end  becomes  enlarged  to 
form  the  beginning  of  the  bulbus  arteriosits. 


Som.     W.D.Seg.Sp.c. 


EC.  Mes. 


Coe. 


Ve.     nch.     Ent.          Spl.     mes.1 


FIG.  52. — TRANSVERSE  SECTION  OF  A  CHICK  EMBRYO  WITH  ABOUT 

TWENTY-EIGHT  SEGMENTS.       (After  Minot.) 

Coe,  coelom.  EC,  ectoderm.  Ent,  entoderm.  Mes,  somatic  mesoderm.  mes* 
splanchnic  mesoderm.  JV,  nephrostome.  nek,  notochord.  Seg*  segment.  Som^ 
somatopleure.  Sp.c,  spinal  chord.  Spl,  splanchnopleure.  Ve,  blood-vessel.  WD, 
Wolffian  duct. 


The  point  of  the  loop  will  develop  into  the 
ventricles  (Fig.  57). 

The  vascular  system. — A  single  pair  of  aortic 
arches  has  already  been  mentioned  as  extend- 
ing from  the  bulbus  arteriosus  to  the  dorsal 
side  of  the  digestive  tract,  where  each  one  is 
continued  to  the  posterior  end  of  the  embryo 
as  a  dorsal  aorta.  Before  the  end  of  this  day 
the  two  dorsal  aortae  unite,  behind  the  head, 


Development  of  the  Second  Day    157 

to  form  a  single  vessel  lying  just  under  the 
notochord  (Fig.  71,  A  O)  ;  but,  after  continu- 
ing for  a  short  distance  towards  the  tail,  this 
single  aorta  again  divides  into  two  vessels, 
from  each  of  which  is  given  off  the  large  vitel- 
line  artery  that  has  already  been  mentioned 
(Fig.  65).  After  giving  off  the  vitelline  ar- 
teries the  dorsal  aortae  continue,  with  greatly 
diminished  calibre,  to  the  tail. 

A  second  pair  of  aortic  arches  is  now  formed 
behind  the  first,  and  even  a  third  pair  may  be 
formed  before  the  close  of  the  second  day,  so 
that  the  front  of  the  bulbus  arteriosus  is  con- 
nected with  the  dorsal  aortae  by  two  or  three 
pairs  of  vessels  (Figs.  65  and  76). 

The  sinus  terminalis  and  the  other  vessels 
of  the  vascular  area  are  now  well  developed,  so 
that  a  real  circulation  of  the  blood  is  possible, 
which  was  not  the  case  for  a  time,  even  after 
the  heart  had  begun  to  beat. 

The  course  of  the  circulation  at  the  end  of 
the  second  day  is,  then,  somewhat  as  follows  : 
the  blood,  after  being  brought  back  by  the 
vitelline  veins,  is  forced,  by  the  contraction  of 
the  heart,  through  the  aortic  arches  into  the 
dorsal  aorta  :  passing  back  through  the  aorta, 
a  small  portion  goes  into  the  tail  of  the  embryo,. 


i58          Vertebrate  Embryology 

but  the  greater  part  passes  out  to  the  vas- 
cular area.  The  blood  that  goes  to  the  vas- 
cular area  through  the  vitelline  arteries  gets 
back  into  the  vitelline  veins  in  two  ways  :  it 
may  pass  directly  to  the  veins  from  the  arteries 
through  the  connecting  capillaries ;  or  it  may 


FIG.  53. — TRANSVERSE  SECTION  THROUGH  THE  HEART  REGION  OF 
AN  EMBRYO  OF  33  HOURS.     (After  Duval.) 

Ao,  aorta.    C,  cavity  of  heart.    MCA  and  MCP,  mesoblastic  part  of  the  heart. 
PC,  pericardial  region  of  body  cavity.     /%,  pharynx.     VA,  auditory  pits. 

pass  into  the  sinus  terminalis,  at  a  middle  point 
on  each  side,  and  then  pass  through  this  large 
vessel  both  forwards  and  backwards :  the 
larger  part  passes  forwards  until  a  point  near 
the  head  is  reached,  when  it  is  returned  to  the 
vitelline  veins  through  two  large  parallel  ves- 
sels. At  this  time  the  blood  that  flows  towards 
the  tail,  in  the  sinus  terminalis,  is  simply  dis- 


Development  of  the  Second  Day    159 

tributed  to  the  vascular  area  in  that  region,  as 
there  is,  as  yet,  no  vessel  connecting  the  pos- 
terior part  of  the  sinus  terminalis  with  the 
vitelline  veins.  These  veins  run  parallel  to 
and  a  little  in  front  of  the  vitelline  arteries. 
The  course  of  the  circulation  at  this  time  may 
be  understood  from  Fig.  56,  which  is  of  a  some- 
what later  period. 

The  Wolffian  duct,  during  this  period,  con- 
tinues  to   elongate  both  anteriorly  and  pos- 


FIG.  54.— TRANSVERSE  SECTION  THROUGH  THE  DORSAL  REGION 
OF  AN  EMBRYO  OF  46  HOURS.     (After  Duval.) 

Ao,  aorta.    CSW,  nephrostome  of  Wolffian  body.     CIV,  Wolffian  duct,    of, 
alimentary  canal. 

teriorly,  and  its  posterior  end  becomes  free 
from  the  mesoblast  and  lies  in  the  space 
between  the  ectoblast  and  mesoblast.  A  small 
lumen  now  appears  near  its  middle  point  and 
gradually  extends  both  forwards  and  back- 
wards. At  a  later  period  (on  the  fourth  day) 
the  duct  opens  into  the  cloaca. 

The  Wolffian  body  makes  its  first  appearance 


i6o          Vertebrate  Embryology 

on  this  day,  but  its  development  will  be  de- 
scribed at  a  later  time. 

The  amnion  usually  makes  its  appearance 
during  the  second  day,  though,  as  has  been 
noticed,  it  may  sometimes  be  seen  as  a  very 
small  rudiment  at  the  end  of  the  first  day. 

As  was  stated  in  the  summary  of  develop- 
ment, the  head-fold  of  the  amnion  is  the  first 
to  appear.  The  mesoblast  in  spreading  does 
not  extend  into  the  region  immediately  in  front 
of  the  head :  this  small  area,  which  consists  of 
but  two  layers,  the  ectoblast  and  the  entoblast, 
is  known  as  the  pro-amnion  (Fig.  46,  pr.  am), 
and  it  is  in  this  place  that  the  head-fold  of  the 
amnion  is  formed ;  therefore  this  head-fold  is, 
for  a  time,  made  up  only  of  ectoblast,  but  at  a 
little  later  period  the  mesoblast  extends  into  it, 
so  that  it,  like  the  tail-  and  lateral-folds,  is  made 
up  of  both  ectoblast  and  mesoblast.  The  actual 
method  of  development  of  the  head-fold  of  the 
amnion  was  sufficiently  described  in  speaking 
of  the  cloth  model  (page  114),  and  attention 
may  be  again  called  to  Fig.  38. 

By  the  end  of  this  day,  the  head  and  neck 
of  the  embryo  are  covered  by  the  amnion  ;  the 
tail-  and  lateral-folds  of  the  amnion  are  well 
started,  but  are  not  so  far  advanced  in  develop- 


Development  of  the  Second  Day    16 1 

ment  as  the  head-fold.  As  will  be  seen  by 
examination  of  Figs.  37  and  38,  the  space  be- 
tween the  two  layers  of  the  amnion  (dotted  in 


FIG.  55.  —  TRANSVERSE  SECTION  THROUGH  A  CHICK  EMBRYO,  TO 
SHOW  A  SLIGHTLY  LATER  STAGE  IN  THE  DEVELOPMENT  OF  THE 

HEART  THAN  IS  SHOWN  IN  FlG.  48.       (After  Minot.) 

Md,  wall  of  medullary  tube,  nek,  notochord.  mstk,  mesothelium.  PA, 
pharynx,  pro.  am,  tip  of  pro-amnion.  en.ht,  endothelial  heart,  m.ht,  muscular 
heart. 

Fig.  37)  is  continuous  with  the  body  or  pleuro- 
peritoneal  cavity. 

The  allantois  may  make  its  appearance  be- 
fore the  close  of  this  day,  but  it  will  be  better 
to  defer  its  description  until  the  following  day's 
development  is  discussed. 


1 62          Vertebrate  Embryology 

SUMMARY 

The   most   important  events  of  the  second 
half  of  the  second  day  are  : 

1.  The  change  in  shape  and  position  of  the 
optic  vesicles. 

2.  The  origin  of  the  unpaired  rudiment  of 
the  cerebral  hemispheres  from  the  front  of  the 
fore-brain. 

3.  The  cranial  flexure  becomes  visible. 

4.  The    auditory   pits   become   deeper   and 
more  pronounced. 

5.  The  curvature  of  the  heart  increases  and 
the  rudiments  of  the  auricles  and  bulbus  arte- 
riosus  appear. 

6.  The  head-fold  advances  rapidly  and  the 
tail-  and  lateral-folds  make  their  appearance. 

7.  The  circulation  of  the   vascular  area   is 
definitely  established. 

8.  The  amnion  covers  the  head  and  neck  of 
the  embryo,  and  its  tail-  and  lateral-folds  are 
well  marked. 

9.  The  first   indication   of   the  allantois  is 
seen. 


CHAPTER  V 

THE  DEVELOPMENT  OF  THE  THIRD  DAY 

SINCE  there  is  no  especial  advantage  in 
dividing  the  third  day  into  two  periods, 
as  was  done  with  the  second  day,  it  will 
be  treated  as  a  single  period. 

Of  all  the  twenty-one  days  of  the  chick's 
embryonic  development,  the  third  is,  perhaps, 
the  most  eventful  in  the  number  of  structures 
that  make  their  appearance. 

There  is  a  marked  increase  in  the  size  of 
the  embryo  and  of  the  blastoderm  during  this 
day,  the  blastoderm  now  covering  about  half 
of  the  surface  of  the  yolk.  There  may  also  be 
noticed  a  corresponding  decrease  in  the  amount 
of  the  white  of  the  egg,  due  either  to  its  direct 
absorption  by  the  blood  vessels  of  the  vascular 
area,  or  to  the  absorption  of  the  yolk  which  is, 
in  turn,  replaced  by  the  white. 

The  diminution  of  the  white  brings  the  vas- 
cular area  close  to  the  inner  surface  of  the 
shell  membrane,  so  that  it  is  now  possible  for 

163 


1 64          Vertebrate  Embryology 

an  aeration  of  the  blood  to  take  place,  and 
the  vascular  area  serves  both  as  an  organ  of 
absorption  and  of  respiration.  In  fact  the 
vascular  area,  at  this  time,  reaches  its  greatest 
activity,  for  while  it  may  become  greater  in 
extent,  it  later  loses  the  function  of  a  respira- 
tory organ  (after  the  formation  of  the  allan- 
tois),  and  serves,  for  the  rest  of  the  period  of 
incubation,  merely  as  an  organ  of  absorption. 
There  are  certain  changes  that  take  place  in 
the  vascular  area  during  the  third  day.  Owing 
to  the  growth  of  the  embryo,  the  vitelline 
veins,  which,  during  the  second  day,  were  some 
distance  in  front  of  the  vitelline  arteries,  are 
brought  nearer  and  nearer  to  these  arteries  un- 
til they  lie  so  close  to  them  that  the  two  ves- 
sels can  hardly  be  distinguished.  During  this 
day  the  sinus  terminalis  reaches  its  greatest 
functional  activity.  The  blood  that  empties 
into  it  from  the  vitelline  arteries  flows,  as  be- 
fore, both  forwards  and  backwards,  that  is, 
towards  the  head  and  towards  the  tail.  The 
blood  that  flows  towards  the  head  usually  gets 
back  into  the  vitelline  veins  through  two  large 
vessels  that  lie  parallel  to  the  long  axis  of  the 
embryo  (Fig.  56)  ;  occasionally,  however,  there 
is  only  one  of  these  vessels,  the  one  which 


Development  of  the  Third  Day    165 

empties  into  the  left  vitelline  vein  ;  and  in  any 
case  the  left  vessel  is  the  larger,  if  two  are 
present.  The  blood  that  flows  backwards  in 
each  half  of  the  sinus  terminalis  empties  into 
a  single  posterior  vessel,  and  through  that  is 
brought  back  to  the  left  vitelline  vein  (Fig. 
56).  This  posterior  vessel,  bringing  blood 
from  the  hinder  half  of  the  sinus  terminalis, 
was  not  present,  it  will  be  remembered,  during 
the  second  day. 

The  folding  off  of  the  embryo  from  the  yolk 
makes  great  progress,  during  this  day,  so  that 
it  is  now  more  clearly  outlined  by  the  deep- 
ening of  the  head-,  tail-,  and  side-folds,  and  is  a 
tubular  body  or  sac  (embryo-sac}  connected 
with  the  yolk-sac  by  a  sort  of  wide  stalk.  By 
examining  Fig.  38,  it  will  be  seen  that  this 
stalk  is  a  double  tube ;  the  inner  tube  or  stalk 
is  known  as  the  splanchnic  stalk,  and  is  con- 
tinuous with  the  now  clearly  defined  digestive 
canal :  the  outer  tube  or  stalk  is  the  somatic 
stalk,  and  its  cavity  is  continuous  with  the 
body-cavity,  while  its  walls  are  a  continuation 
of  the  somatopleure  (study  carefully  Figs.  37 
and  38). 

A  remarkable  change  in  position  takes  place 
during  this  day.  Up  to  the  close  of  the  second 


1 66          Vertebrate  Embryology 


day,  the  embryo  has  been  lying  "  face  down- 
wards "  upon  the  yolk.  During  the  third  day, 
the  embryo  turns  over  until  it  lies  on  its  left 


B.C, 


Ht 


AO 


9.T 


0m.  A. 


Om 


FIG.  56.— DIAGRAM  OF  THE  CIRCULATION  OF  A  CHICK  EMBRYO 

AT  THE  END  OF  THE  THIRD  DAY  OF  INCUBATION,  AS  SEEN  FROM  THE 

UNDER  SIDE.  (After  Minot.)  The  embryo,  with  the  exception  of 
the  heart,  is  dotted  ;  the  veins  are  black. 

A  0,  aorta.  A  re,  aortic  arches,  card,  cardinal  vein.  DC,  duct  of  Cuvier.  7/2, 
heart.  Jug,  jugular  vein.  Om.A,  vitelline  artery.  Om.V^  vitelline  vein.  ST. 
sinus  terminalis.  S^  sinus  venosus. 

side  (Figs.  57  and  80).  The  head,  which  is 
the  first  part  to  be  affected  by  this  change, 
begins  to  turn  early  in  this  day,  and  by  the 


Development  of  the  Third  Day    167 

middle  of  the  day  the  body  is  twisted  so  that, 
on  looking  down  upon  the  embryo,  the  anterior 
end  is  seen  in  profile  while  the  posterior  end  is 
still  seen  from  the  dorsal  side  (Fig.  57).  By 
the  end  of  the  third,  or  early  in  the  fourth  day 
the  embryo  has  completed  the  change  in  posi- 
tion. At  the  same  time  that  the  embryo  is 
turning  over  to  its  left  side,  a  marked  curva- 
ture of  the  body  begins  and  becomes  so  great, 
at  a  later  stage,  that  the  head  and  tail  almost 
touch  each  other. 

As  the  embryo  turns  to  its  left  side,  the  vi- 
telline  vein  of  that  side  becomes  much  larger 
than  the  other  vein,  and  the  right  vitelline  vein 
dwindles  in  size  and  at  last  disappears. 

The  cranial  flexure  increases  very  markedly, 
during  this  period,  so  that  the  fore-brain  now 
lies  ventral  to  the  hind-brain,  and  the  mid- 
brain  is  often  the  most  anterior  part  of  the 
head,  along  a  straight  axis  through  the  centre 
of  the  embryo  (Fig.  57). 

The  amnion. — As  the  amnion  becomes  prac- 
tically complete  during  this  day,  its  entire  his- 
tory will  be  given  so  that  it  need  not  be  more 
than  referred  to  again. 

At  the  end  of  the  second  day,  it  will  be  re- 
membered, the  head-fold  of  the  amnion  covered 


1 68          Vertebrate  Embryology 

the  head  and  neck  of  the  embryo,  while  the 
tail-  and  lateral-folds  had  started  to  develop, 
but  were  not  nearly  so  far  advanced  as  the 
head-fold.  By  the  end  of  the  third  day,  the 
different  folds  of  the  amnion  have  met,  and 
covered  all  of  the  embryo  except  a  small  spot 
at  the  posterior  end.  During  the  fourth  day 
the  amnion  becomes  complete  and  entirely 
covers  the  embryo  (Figs.  37  and  57).  As  the 
head-,  tail-,  and  side-folds  of  the  amnion  meet, 
their  outer  layers  all  fuse  together  to  form  a 
continuous  sheet,  the  outer  or  false  amnion 
(the  serous  membrane)  ;  while  the  inner  layers 
fuse  to  form  the  inner  or  true  amnion  (Fig. 
38).  Between  the  inner  and  outer  layers  of 
the  amnion  is  a  space,  continuous,  as  has  been 
said,  with  the  body-cavity,  into  which  the  al- 
lantois,  presently  to  be  described,  grows. 

The  space  between  the  true  amnion  and  the 
embryo  is  the  amniotic  cavity ;  and  in  it  is 
soon  developed  a  watery  fluid,  which  is,  at 
first,  very  small  in  quantity,  but  which  later 
increases  enormously. 

Up  to  the  fifth  day,  the  amniotic  cavity  is 
very  small,  so  that  the  true  amnion  invests  the 
embryo  quite  closely ;  but  during  the  later 
days  of  incubation,  the  amniotic  fluid  becomes 


Development  of  the  Third  Day    169 

so  abundant  that  the  embryo  can  move  freely 
in  the  amniotic  cavity  ;  and  a  rocking  motion 
is  given  the  embryo  by  the  contraction  of 
muscle  fibres  that  are  developed  in  the  am- 
niotic membrane.  What  the  purpose  of  this 
rocking  motion  may  be  is  not  easy  to  say,  but 
the  chief  object  of  the  amnion  and  its  con- 
tained fluid  is  probably  for  the  protection  of 
the  soft  and  delicate  embryo. 

The  amnion  is  not  really  a  part  of  the  embryo 
proper,  and  is  left  in  the  shell  at  the  time  of 
hatching.  It  is  a  very  characteristic  structure 
in  the  development  of  the  three  higher  groups 
of  Vertebrates, — Reptiles,  Birds,  and  Mammals. 

The  allantois. — Although  the  allantois  origi- 
nates during  the  second  day  and  continues  to 
increase  in  size  throughout  a  greater  part  of 
the  period  of  incubation,  it  will  be  convenient 
to  describe  its  complete  history  at  this  point, 
so  that  it  need  be  merely  mentioned  at  sub- 
sequent periods.  We  cannot  do  better  than 
quote  at  length  from  the  account  of  the  de- 
velopment of  the  allantois  given  by  Marshall. 

"  The  allantois  is  really  an  appendage  of  the  alimen- 
tary canal,  arising  as  an  outgrowth  of  its  ventral  wall,  in 
front  of  the  cloaca;  it  is  therefore  lined  by  hypoblast, 
like  all  other  outgrowths  of  the  mesenteron,  while  the 


170          Vertebrate  Embryology 

rest  of  the  thickness  of  its  walls  is  formed  by  the  splanch- 
nopleuric  mesoblast. 

"  The  allantois  of  the  chick  is  homologous  with  the 
bladder  of  the  frog.  It  differs  mainly  from  this  in  the 
fact  that,  while  arising  in  the  same  manner,  it  is  not  con- 
fined within  the  body  of  the  embryo,  but,  growing  rapidly, 
passes  out  beyond  this  as  a  thin-walled  vascular  sac  (Figs. 
38,  72,  and  80),  which  spreads  out  in  close  contact  with 
the  inner  surface  of  the  egg-shell,  and  acts  as  the  respi- 
ratory organ  of  the  embryo  during  the  greater  part  of  its 
development. 

"  In  the  chick  the  allantois  commences  to  form  about 
the  middle  of  the  second  day.  At  this  time  the  tail  fold 
is  not  yet  established,  so  that  the  allantois  (Fig.  51,  Al.) 
appears  at  first  as  a  pocket-like  fold  of  the  splanchno- 
pleure,  lying  a  short  way  behind  the  embryo,  and  with 
its  cavity  opening  ventralwards. 

"  On  the  formation  of  the  tail  fold,  early  on  the  third 
day,  the  part  of  the  splanchnopleure  from  which  the 
allantois  arises  becomes  doubled  forwards  under  the 
embryo  to  form  the  ventral  wall  of  the  gut,  and  the  al- 
lantois now  appears  as  a  saccular  depression  of  the 
ventral  wall  of  the  hind-gut  (Fig.  38,  C). 

"  During  the  third  day  the  allantois  increases  con- 
siderably in  size,  projecting  downwards  and  forwards, 
as  a  hollow,  thick-walled  bud  from  the  ventral  surface 
of  the  hind-gut,  into  the  body  cavity,  or  space  between 
the  somatic  and  splanchnic  layers  of  the  mesoblast. 
During  the  fourth  day,  by  its  further  growth,  the  allan- 
tois passes  out  beyond  the  embryo,  and  turns  up  along 
its  right  side,  into  the  space  between  the  two  layers  of 
the  amnion,  which,  from  the  mode  of  formation  of  the 


Development  of  the  Third  Day    171 

amnion,  is  directly  continuous  with  the  body  cavity  of 
the  embryo  (Figs.  37,  G-K,  and  38,  C). 

"  On  the  fifth  and  following  days  the  allantois  grows 
rapidly;  from  the  first  it  is  very  vascular,  and  the  blood 
vessels  now  increase  greatly  in  size;  the  arteries,  which 
lie  in  its  superficial  layer,  are  derived  directly  from  the 
aorta  (Fig.  76);  while  the  veins,  V  A,  which  lie  in  its 
inner  or  deeper  layer,  join  the  vitelline  veins  from  the 
yolk-sac,  and,  passing  through  the  liver,  reach  the  heart. 
By  the  seventh  or  eighth  day  (Fig.  38,  D)  the  allantois 
has  spread  all  around  the  upper  half  of  the  egg,  covering 
over  the  embryo,  and  extending  half  around  the  yolk-sac 
as  well.  It  is  still  saccular,  and  its  cavity  contains  fluid. 
Its  outer  wall  lies  in  very  close  contact  with  the  outer 
layer  of  the  amnion,  or  false  amnion,  and  soon  fuses  with 
this  completely,  so  that  from  this  time  the  allantois  lies 
in  close  contact  with  the  shell  membrane. 

"  In  its  further  growth  the  allantois  does  not  follow 
the  yolk-sac;  but,  keeping  close  to  the  egg-shell  arid 
carrying  the  somatopleure  before  it,  it  extends  so  as 
gradually  to  enclose  the  mass  of  white,  which  still  remains 
on  the  under  surface  and  near  the  small  end  of  the  egg. 
The  allantois,  about  the  sixteenth  day,  completely  en- 
closes this  plug  of  white  or  albumen,  and  from  this  time 
the  absorption  of  the  plug  proceeds  rapidly,  the  albumen 
being  apparently  carried  by  the  allantoic  vessels  to  the 
embryo,  and  aiding  in  its  nutrition. 

"  Towards  the  close  of  incubation  deposits  of  urates 
occur  in  the  cavity  of  the  allantois,  indicating  that  it 
serves  as  a  receptacle  for  the  excretory  matters  formed 
within  the  embryo  itself,  as  well  as  a  respiratory  organ 
in  the  more  restricted  sense  of  the  term. 


172          Vertebrate  Embryology 

"  Shortly  before  the  time  of  hatching  the  allantoic 
vessels  become  constricted,  by  the  closure  of  the  body 
walls  at  the  umbilicus. 

"The  allantois  itself  shrivels  up,  and  is  cast  off  as  the 
chick  works  its  way  out  of  the  shell." 

In  the  highest  group  of  Vertebrates,  the 
Mammals,  the  allantois  becomes  developed 
into  a  structure  known  as  the  placenta,  by 
which  the  embryo  is  attached  to  the  parental 
uterus,  and  through  which  it  receives  nourish- 
ment from  its  mother. 

The  allantois,  then,  like  the  amnion,  is  an 
extra-embryonic  structure,  and  is  cast  aside  at 
the  time  of  hatching. 

The  brain. — Since  the  limits  of  this  book 
will  permit  the  discussion  of  only  the  most  im- 
portant points  in  the  development  of  the  brain, 
and  since  the  development  of  the  important 
features  in  the  chick  is  essentially  the  same  as 
in  the  frog,  the  reader  is  referred  to  the  first 
part  of  this  book  (pages  31-40)  for  a  descrip- 
tion of  the  development  of  the  brain.  There 
are  some  points  of  difference  which  might  be 
mentioned  ;  for  example  :  the  cerebellum  in 
the  frog  remains  very  small  and  inconspicuous 
throughout  life,  while  in  the  chick  it  eventually 
becomes  very  large,  though  for  the  first  part  of 


Development  of  the  Third  Day    173 

the  period  of  incubation  it  is  as  small,  relatively, 
as  in  the  frog  ;  again  :  the  olfactory  lobes  in 
the  frog  are  at  first  separate,  but  later  fuse  to- 
gether, while  in  the  chick  they  remain  distinct 
throughout  life.  There  are  differences,  of 
course,  in  the  relative  sizes  of  the  various  parts 
of  the  two  brains,  but,  as  has  been  said,  the 
main  features  in  development  are  essentially 
the  same  in  the  two  forms,  and  a  more  detailed 
description,  if  desired,  may  be  found  in  larger 
works. 

The  peripheral  nervous  system. — In  the  de- 
velopment of  the  cranial  and  spinal  nerves 
there  is  such  close  resemblance  between  the 
frog  (page  40)  and  the  chick  that  but  little 
need  be  said  at  this  place.  They  arise  (the 
cranial  nerves,  perhaps,  a  little  earlier  than 
the  spinal)  during  the  latter  part  of  the  first 
or  the  early  part  of  the  second  day  (Fig.  53), 
before  the  medullary  folds  have  fused  together 
along  the  mid-dorsal  line.  As  in  the  frog,  there 
are  many  points  in  the  development  of  the 
peripheral  nervous  system  that  are  still  under 
discussion. 

The  sympathetic  nervous  system. — The  origin 
of  the  sympathetic  nervous  system  in  the  chick 
has  been  the  subject  of  much  debate.  It  is 


174          Vertebrate  Embryology 

probably  derived  from  the  spinal  nervous  sys- 
tem, and  is  hence  merely  a  specialized  part 
of  that  system.  According  to  this  view  it 
originates  as  a  series  of  outgrowths  from  the 
spinal  ganglia,  which  outgrowths  extend  in- 
ward until  they  nearly  reach  the  dorsal  aorta : 
at  their  inner  ends  they  become  enlarged  to 
form  the  sympathetic  ganglia,  and  these  ganglia 
send  out  processes  which  fuse  to  form  the 
longitudinal  commissures. 

THE    DEVELOPMENT   OF  THE   SENSE   ORGANS 

The  development  of  the  sense  organs,  the 
eye,  ear,  and  nose,  though,  in  most  respects, 
similar  to  the  development  of  the  same  organs 
in  the  frog,  will  be  described  in  more  detail 
than  was  done  in  connection  with  the  frog. 

The  eye. — Although  it  begins  in  the  early 
part  of  the  second  day  and  is  not  completed 
until  late  in  the  period  of  incubation,  it  will  be 
most  convenient  to  describe  the  entire  develop- 
ment of  the  eye  at  this  point,  rather  than  wait 
until  the  development  of  the  following  days  is 
discussed.  In  any  case,  the  greater  part  of  the 
changes  here  described  take  place  before  the 
end  of  the  third  day. 


JTIG  57.— SURFACE  VIEW  OF  AN  EMBRYO  OF  52  HOURS.  (After 
Duval.) 

Aom,  vitelline  artery.  C,  heart.  FO,  olfactory  pit.  LC,  lateral  limits  of 
body.  AT,  tail.  ^2,  mid-brain.  Vva  and  Vvp,  antenor  and  posterior  branches 
of  the  vitelline  vein.  Vo,  eye. 

175 


1 76          Vertebrate  Embryology 

As  has  already  been  described,  the  first  in- 
dication of  the  formation  of  the  eye  is  seen  on 
the  second  day,  when  the  optic  vesicles  are 
pushed  out  from  the  sides  of  the  fore-brain. 
By  the  end  of  the  second  day  these  vesicles 
are  very  prominent,  and  are  constricted  at  their 
bases  to  a  narrow  stalk,  known  as  the  optic 
stalk  (Fig.  60,  O  S).  The  optic  stalk  is  hollow 
and  connects  the  optic  vesicle  with  the  lower 
part  of  the  fore-brain.  At  the  end  of  the  sec- 
ond day,  a  slight  thickening  is  seen  in  the 
superficial  ectoblast  at  the  nearest  point  to 
the  outer  wall  of  the  optic  vesicle  (Fig.  59, 
L).  This  is  the  first  indication  of  the  lens. 
This  thickening  becomes  pitted  in  to  form,  by 
the  fusion  of  the  lips  of  the  pit,  a  closed  sac 
(Figs.  59,  L,  and  60,  L),  the  lens  vesicle.  The 
lens  vesicle,  during  the  third  day,  separates 
from  the  superficial  ectoblast,  and  the  latter  be- 
comes again  a  continuous  layer  (Fig.  60,  L). 
The  outer  wall  of  the  lens  vesicle,  after  its 
separation  from  the  ectoblast,  remains  thin  ; 
while  the  inner  wall  becomes  thicker  and 
thicker,  by  the  growth  and  elongation  of  its 
constituent  cells,  until,  on  the  fourth  day,  it 
comes  in  contact  with 'the  thin  front  wall  and 
entirely  obliterates  the  cavity  of  the  vesicle. 


Development  of  the  Third  Day    177 

While  the  cells  of  the  inner  wall  are  elongating 
until  they  form  what  might  almost  be  called 


Ao.D 


EC 


mes. 


f.b. 


FIG.  58. — TRANSVERSE  SECTION  THROUGH  THE  ANTE- 
RIOR REGION  OF  A  CHICK  EMBRYO  WITH  ABOUT  TWENTY- 
EIGHT  SEGMENTS.  (After  Minot.) 

Ao.,  trunk  of  the  aorta.  Ao.D.,  descending  aorta.  Ao.*,  second 
aortic  arch,  card.,  anterior  cardinal  vein.  cl.II.,  second  entodermal 
gill-pouch.  EC.)  ectoderm,  f.b.,  fore-brain,  h.b.,  hind-brain.  Hi., 
heart,  mes.,  mesoderm.  My.,  muscle  plate,  nek.,  notochord.  Op., 
optic  vesicle.  Ph.,  pharynx. 


fibres,  the  cells  of  the  outer  wall,  except  at  the 
periphery  of  the  lens,  where  they  become  con- 


178  Vertebrate  Embryology 

tinuous  with  the  cells  of  the  inner  wall,  are  be- 
coming flatter  and  flatter,  until  they  form  a 
mere  membrane :  this  membrane  forms  the 
epithelial  lining  of  the  lens  capsule.  The  lens 
capsule  is  probably  a  cuticular  membrane  se- 
creted by  the  epithelial  cells  of  the  lens  vesicle, 
though  it  has  been  held,  by  some,  to  be  of 
mesoblastic  origin. 

As  the  ectoblast  thickens  to  form  the  lens 
vesicle,  the  optic  vesicle  becomes  invaginated, 
from  the  side  next  to  the  lens  vesicle,  just  as  a 
hollow  rubber  ball  might  be  pushed  in  on  one 
side  with  the  finger  (Figs.  59  and  60).  The 
invaginated  optic  vesicle  is  now  known  as  the 
optic  cup,  o  c,  and  consists,  naturally,  of  two 
walls :  of  these  walls,  the  inner  soon  becomes 
the  thicker,  and  this  inequality  in  the  thickness 
of  the  two  walls  becomes  greater  as  develop- 
ment proceeds.  The  two  walls  of  the  optic 
cup  gradually  approach  each  other  until  they 
meet  and  thus  obliterate  the  cavity  of  the 
original  optic  vesicle  (Fig.  60). 

The  lips  of  the  optic  cup  lie  close  to  the 
circumference  of  the  lens,  and  by  their  growth 
the  depth  of  the  cup  is  constantly  increased. 
This  growth  of  the  lips  of  the  optic  cup  takes 
place  at  all  points  except  one  :  at  a  point  near 


Development  of  the  Third  Day    179 

the  optic  stalk  the  lips  do  not  increase  in 
height,  and  a  cleft  or  fissure,  the  choroid 
fissure  (Fig.  64,  O  H),  is  left  at  that  place. 
The  exact  method  of  formation  of  the  cho- 
roid fissure  is  not  easy  to  determine.  The 
invagination  of  the  optic  vesicle  to  form  the 
optic  cup  may  be  partly  caused  by  the  me- 
chanical pushing  inward  of  the  lens,  but  it  is 
probably  also  caused  by  the  unequal  growth 
of  the  walls  of  the  vesicle.  In  a  similar  man- 
ner the  unequal  growth  of  the  lips  of  the  cup 
may  cause  the  formation  of  the  choroid  fissure  ; 
but  there  is  some  evidence  to  show  that  the 
fissure  may  be,  in  part,  the  result  of  the  growth 
of  the  fibres  of  the  optic  nerve.  The  choroid 
fissure  is  a  very  transient  structure ;  by  the 
sixth  day  its  edges  have  met,  and  shortly  after- 
wards they  fuse,  so  that  by  the  ninth  day  no 
trace  of  the  fissure  remains. 

The  inner  wall  of  the  cup,  which  is  the 
thicker  almost  from  the  first,  by  the  third  day 
consists  of  elongated,  nucleated  cells  arranged 
in  a  single  row  perpendicular  to  the  surface  of 
the  cup.  The  thickness  of  this  inner  wall  con- 
tinues to  increase,  and  by  a  process  of  histo- 
logical  differentiation  that  is  difficult  to  follow, 
it  is  converted  into  the  retina.  The  outer 


180          Vertebrate  Embryology 

wall  of  the  optic  cup  becomes  thinner,  as  the 
inner  wall  increases  in  thickness,  until  it  is  re- 


Epen. 


f.b. 


FIG.  59. — TRANSVERSE  SECTION  THROUGH  THE  ANTE- 
RIOR REGION  OF  A  CHICK  EMBRYO  WITH  ABOUT  TWENTY- 
EIGHT  SEGMENTS.  (After  Minot.) 

Ao.D.,  descending  aorta.  A0.1,  first  aortic  arch.  Ao. 2.  second 
aortic  arch,  card.,  anterior  cardinal  vein.  cl.I.,  first  gill  cleft.  cl.II., 
second  gill  cleft.  EC.,  ectoderm.  Ent.,  entoderm.  Epen.,  roof  of 
hind-brain,  f.b.,  fore-brain,  h.b.,  hind-brain.  L.,  invagination  of 
lens.  Mdb.,  mandibular  arch,  mes.,  mesoderm.  nch.,  notochord. 
Op.,  optic  vesicle.  Ph.,  pharynx.  Ret.,  retina. 

duced  to  a  single  layer  of  flattened  cells  which 
soon  become  darkly  pigmented,  and  form  the 


Development  of  the  Third  Day    181 

layer  of  pigmented  cells  that  lies  close  to  the 
outer  ends  of  the  rods  and  cones.  The  whole 
of  the  sensory  part  of  the  retina  is,  therefore, 
derived  from  the  inner  layer  or  wall  of  the 
optic  cup. 

It  is  sometimes  stated  that  the  optic  nerve  is 
formed  by  the  hollow  stalk  of  the  optic  cup  ; 
but  it  is  probable  that  it  is  formed  by  an  out- 
growth of  cells  from  the  retina,  this  outgrowth 
extending  along  the  optic  stalk  to  the  brain, 
and  forming  the  fibres  of  the  optic  nerve. 
The  growth  of  these  fibres  may  have,  as  has 
been  mentioned,  something  to  do  with  the 
formation  of  the  choroid  fissure. 

The  choroid  and  sclerotic  coats  are  formed 
from  a  layer  of  condensed  mesoblast  that  col- 
lects around  the  optic  cup  :  and  an  ingrowth 
of  mesoblast,  through  the  choroid  fissure,  is 
converted  into  the  vitreous  humor. 

The  retina  does  not,  of  course,  cover  the 
entire  inner  surface  of  the  optic  cup.  The 
edges  of  the  optic  cup,  beyond  the  limits  of 
the  retina,  form  a  part  of  the  iris.  In  this  re- 
gion the  two  layers  of  the  cup  completely  fuse, 
and  their  cells  become  deeply  pigmented. 
Fusion  now  takes  place  between  this  layer  of 
pigmented  cells  and  the  choroid  layer  that  has 


1 82          Vertebrate  Embryology 

formed^  outside  of  it,  and,  by  the  inward  growth 
of  what  we  may  now  call  the  iris,  the  opening 
of  the  optic  cup  is  reduced  to  a  small  circular 
opening,  the//////. 


FB 


FIG.  60. — TRANSVERSE  SECTION  THROUGH  THE  FORE- 
BRAIN  OF  A  CHICK  OF  50  TO  60  HOURS'  INCUBATION.  To 
illustrate  the  formation  of  the  optic  cup,  lens  vesicle,  etc. 

A,  the  amnion.  EP,  superficial  ectoblast,  FB,  cavity  of  the 
fore-brain.  Z,  Lens.  L  Y.  lens  vesicle.  M,  mesoblast.  OC,  cavity 
of  the  optic  cup.  OS,  stalk  connecting  the  optic  cup  with  the  fore- 
brain.  OV,  remains  of  the  cavity  of  the  original  optic  vesicle. 

The  pecten  originates  as  a  vascular  tuft  of 
mesoblast  which  grows  into  the  cavity  of  the 
optic  cup  through  the  choroid  fissure,  near  the 
origin  of  the  optic  stalk.  It  is  first  seen  at 
about  the  fifth  day,  and  by  the  tenth  day  it 


Development  of  the  Third  Day    183 

becomes  folded  to  form  the  fan-like  structure 
of  the  adult  pecten.  Before  the  time  of  hatch- 
ing it  becomes  deeply  pigmented.  The  pec- 
ten  is  a  structure  characteristic  of  the  eyes  of 
birds  and  of  many  reptiles  :  its  exact  function 
is  not  known  with  certainty  (Fig.  61). 

The  cornea,  which  is  apparently  simply  a 
continuation  of  the  sclerotic  coat,  is  made  up 
of  mesoblast  which  grows  in  between  the  lens 
and  the  superficial  epithelium.  It  is,  at  first, 
structureless,  but  certain  of  the  mesoblast 
cells  become  converted  into  the  corneal  cor- 
puscles. These  corpuscles  form  a  layer  in  the 
middle  part  of  the  thickness  of  the  cornea, 
while  the  inner  and  outer  surfaces  remain 
structureless  and  form  the  anterior  and  poste- 
rior membranes.  The  layer  of  surface  epithe- 
lium persists  as  the  conjunctival  epithelium. 

The  anterior  chamber  of  the  eye  forms 
between  the  lens  and  the  cornea,  and  in 
this  chamber  the  aqueous  humor  collects. 

"  The  eyelids  are  folds  of  integument  around  the 
eye;  there  are  three  of  them,  an  upper  and  a  lower 
eyelid,  and  the  third  eyelid  or  nictitating  membrane 
which  arises  on  the  inner  or  nasal  side  of  the  eye. 
The  lacrymal  glands  are  solid  ingrowths  of  the  con- 
junctival epithelium,  which  appear  on  the  eighth 


184          Vertebrate  Embryology 

day.  The  lacrymal  duct  is  also  at  first  solid:  it  ap- 
pears as  a  ridge  of  epidermis,  along  the  line  of  the 
lacrymal  groove,  extending  from  the  eye  to  the  ol- 
factory pit.  This  ridge  sinks  into  the  mesoblast,  and 
soon  splits  off  from  the  epiblast  for  a  greater  part 
of  its  length,  but  remains  attached  at  its  ends  to  the 


set 


cl.p 


pet 


FIG.  61. — THE  EYE  OF  A  BIRD  (COLUMBA  LIVIA).  A,  in  sagittal 
section  ;  B,  external  view  of  entire  organ.  (After  Parker  and  Has- 
well,  from  Vogt  and  Yung.) 

en,  cornea,    ch,  choroid.     cl.pr,  ciliary  process,     ir,  iris.    /,  lens,    opt.nv, 
optic  nerve,    pet,  pecten.     rt,  retina,    scl,  sclerotic,    scl.pl,  sclerotic  plates. 

lower  eyelid  and  to  the  wall  of  the  olfactory  pit  re- 
spectively. About  the  twelfth  day  it  acquires  a 
central  lumen,  and  becomes  the  tubular  duct." ' 

The  ear.     The  ears  begin  about  the  middle 
of  the    second  day,    as   has  been    mentioned, 

1  Marshall. 


Development  of  the  Third  Day    185 

as  a  pair  of  small  pits  pushed  in  from  the 
surface  ectoblast,in  the  region  of  the  hind-brain, 
(Fig.  47,  V  A).  These  auditory  pits  rapidly 
deepen  and,  by  the  end  of  the  third  day,  they 
close  together  and  become  entirely  separate 
from  the  surface  ectoblast  which  fuses  over 
them  so  that  they  are  not  visible  from  the 
surface  (Fig.  62,  Ot.d.).  These  closed  cavities, 
lined  with  epithelium,  are  the  auditory  or  otic 
vesicles  and  from  them,  by  a  process  of  twisting 
and  unequal  growth,  the  membranous  labyrinths 
of  the  ears  are  formed.  The  ends  of  the  audi- 
tory nerves  very  soon  come  in  contact  with 
the  epithelial  linings  of  the  auditory  vesicles, 
and  by  the  early  part  of  the  third  day  they 
have  fused  with  them.  The  places  where 
this  fusion  occurs  will  be  subsequently  de- 
veloped into  the  special  patches  of  sensory 
epithelium  found  in  the  adult  ear. 

The  development  of  the  tympanic  mem- 
brane, tympanic  cavity,  and  Eustachian  tube 
will  be  described  in  another  place,  when  the 
fate  of  the  gill  arches  and  clefts,  is  described. 

It  will  be  remembered  that  the  auditory 
vesicle  in  the  frog  was  formed  from  the 
inner  or  nervous  layer  of  epithelium,  and 
that  the  vesicle  was  never  open  to  the 


1 86          Vertebrate  Embryology 

exterior;  while  in  the  chick  the  entire  thick- 
ness   of    the    epithelium    is    involved    in    the 


h.b. 


Ot.d 


mes 


f.b. 


FIG.  62. — TRANSVERSE  SECTION  THROUGH  THE  ANTE- 
RIOR REGION  OF  A  CHICK  EMBRYO  OF  ABOUT  TWENTY- 
EIGHT  SEGMENTS.  (After  Minot.) 

A o.D.,  descending  aorta.  A0.2.  second  aortic  arch,  card.,  ante- 
rior cardinal  vein,  cl.pl. ,  closing  plate,  cl.l,  first  gill  pouch.  EC., 
ectoderm.  Epen.,  roof  of  hind-brain,  f.b.,  fore-brain,  h.b.,  hind- 
brain,  mes.,  mesoderm.  nek.,  notochord.  Op.,  optic  vesicle.  Ot.d., 
right  otocyst  (ear  vesicle).  Ot.s.,  left  otocyst.  Ph.,  pharynx. 

formation    of    the    auditory    pits,    and    after 
the  pits  become  closed  to  form    the    vesicles 


Development  of  the  Third  Day    187 

the  superficial  epithelium  once  more  be- 
comes continuous. 

The  nose.  The  olfactory  organs  begin,  in 
the  early  part  of  the  third  day,  as  two 
thickenings  of  epithelium  on  the  under 
side  of  the  fore  part  of  the  head.  These 
thickened  patches  soon  become  pushed  in 
to  form  pits,  the  olfactory  pits,  and  the 
olfactory  nerves  very  early  fuse  with  the 
inner  walls  of  the  pits.  The  olfactory  pits 
are  formed  in  the  same  way  as  are  the 
auditory  pits  and  the  pits  that  form  the  lens 
vesicles  of  the  eyes,  but  while  the  lens  and 
auditory  pits  become  closed  completely,  the 
olfactory  pits  remain  permanently  open  to 
the  exterior  as  the  external  nares  or  nostrils 
(Fig.  64,  OK). 

The  epithelial  lining  of  the  olfactory  pit 
becomes  folded  and  wrinkled  to  form  the 
sensory  epithelium  of  the  nose.  The  pos- 
terior nares,  or  the  opening  of  the  nose  into 
the  back  part  of  the  mouth,  is  a  distinct 
formation,  and  appears,  about  the  begin- 
ning of  the  fourth  day,  as  a  groove  leading 
from  the  nasal  pit  to  the  outer  and  ante- 
rior angle  of  the  stomodaeum.  This  groove, 
lying  between  the  fronto-nasal  process  (the 


1 88          Vertebrate  Embryology 

triangular  part  of  the  face,  between  the 
two  nasal  grooves)  and  the  maxillary  arch 
(forming  the  upper  jaw),  becomes  deeper, 
and,  during  the  fifth  day,  is  converted  into 
a  closed  tube,  by  the  fusion  of  its  edges, 
the  above-mentioned  fronto-nasal  process  and 
maxillary  arch.  The  groove  is  thus  convert- 
ed into  a  tube  leading  from  the  nose  into 
the  front  part  of  the  mouth  cavity.  By  the 
forward  growth  of  the  beak,  and  the  for- 
mation of  a  horizontal  septum,  the  palatine 
bone,  the  opening  of  this  tube,  the  posterior 
nares,  comes  to  lie  in  the  back  rather  than 
in  the  front  part  of  the  oral  cavity  (Fig.  64.) 

In  the  development  of  the  sense  organs, 
the  eye,  ear,  and  nose,  there  are  many  points 
in  common,  but  it  should  be  especially  noted 
that  in  all  three  of  these  organs  the  essen- 
tially sensory  parts,  in  each  case,  are  derived 
either  directly  or  indirectly  from  the  ectoblast. 

The  Visceral  Clefts  and  Arches.  Owing  to 
the  unequal  rates  of  growth  of  the  different 
parts  of  the  chick,  the  relative  positions  of 
the  various  organs  are  constantly  changing. 
During  the  second  day,  it  will  be  remembered, 
the  heart  was  formed  in  the  mesoblast,  under 
the  anterior  end  of  the  digestive  tract  or  mes- 


Development  of  the  Third  Day    189 

enteron  (Fig.  49,  C).  During  the  third  day 
the  heart  has  shifted  its  position  so  far  to  the 
rear  that  there  is  a  distinct  space  between  it 
and  the  now  more  sharply  defined  head  (Fig. 
57)  :  this  space  may  be  called  the  neck;  in  this 
region  there  has  been  no  cleavage  of  the 
mesoblast,  so  that  the  three  layers,  the  ento- 
blast,  mesoblast,  and  ectoblast  form  one  con- 
tinuous layer  of  tissue  as  we  pass  outwards 
from  the  fore-gut  or  pharynx  to  the  exterior. 

The  entoblastic  lining  of  the  pharynx, 
during  the  latter  part  of  the  second  or  early 
part  of  the  third  day,  becomes  pushed  out, 
on  each  side,  as  four  narrow  pouches,  the 
visceral  or  gill  pouches,  similar  to  the  five 
pouches  that  have  been  described  (pages 
51  and  52)  in  connection  with  the  frog. 

The  first  three  of  these  pouches,  during 
the  third  and  fourth  days,  open  to  the 
exterior,  their  entoblastic  walls  fusing  with 
the  surface  ectoblast  (Fig.  63,  fb).  Each 
gill,  branchial  or  visceral  cleft,  as  it  is  vari- 
ously called,  is  an  actual,  narrow  chink  opening 
from  the  anterior  end  of  the  digestive  tract 
to  the  exterior.  Owing  to  the  curvature  of 
the  neck,  the  clefts  are  not  parallel  to  each 
other,  but  converge  slightly  towards  a  point 


i9°          Vertebrate  Embryology 

ventral  to  the  middle  part  of  the  neck  (Fig. 
72).  Although  the  visceral  clefts  may  be 
seen,  without  difficulty,  in  favorable  whole 
mounts  of  chicks  of  the  proper  age,  they  are 
quite  small,  and  show  better  in  horizontal 
sections  (Fig.  63),  or  in  chicks  that  have 
been  dissected  so  as  to  lay  open  the  cavity 
of  the  pharynx. 

There  has  been  considerable  discussion  in 
regard  to  the  visceral  clefts,  some  workers 
holding  that  none  of  the  clefts  actually  open 
to  the  exterior ;  but  it  seems  fairly  certain 
that  all  of  the  clefts  normally  open  to  the 
exterior,  except  the  last  or  most  posterior 
one.  There  is  also  some  discussion  as  to 
the  time  of  opening  and  closing  of  the 
branchial  clefts :  while  there  is  probably  a 
good  deal  of  individual  variation  in  this  re- 
spect, it  seems  likely  that  none  of  the  clefts 
open  to  the  exterior  before  the  early  part  of 
the  third  day,  and  that  they  have  all  closed 
before  the  beginning  of  the  sixth  day.  It 
must  not  be  forgotten  that  when  we  speak 
of  the  development  of,  say,  the  fifth  day, 
we  mean  the  average  state  of  development 
reached  by  chicks  during  that  number  of  days 
of  incubation. 


Development  of  the  Third  Day    191 

As  in  the  case  of  the  frog,  the  most  an- 
terior, and  first  formed  gill  cleft  is  called  the 
Jiyomandibular  cleft,  while  the  others,  from 
before  back,  are  the  first,  second  and  third 
gill  clefts.  In  the  frog,  it  will  be  remembered, 
there  were  five  pairs  of  visceral  clefts.  The 
fate  of  the  visceral  clefts  will  be  discussed 
a  little  later. 

The  parts  of  the  side  walls  of  the  pharynx 
between  the  gill  clefts,  and  also  the  anterior 
border  of  the  hyomandibular  cleft  and  the 
posterior  edge  of  the  third  or  last  cleft, 
become  somewhat  swollen  and  rounded,  and 
are  known  as  the  gill  arches.  (Figs.  63,  A  B, 
72).  As  in  the  frog,  again,  the  first  arch  is 
known  as  the  mandibular,  the  second  arch  as 
the  hyoid,  and  the  other  arches  as  \hzfirst, 
second,  and  third. 

In  development  and  structure,  then,  the 
visceral  arches  and  clefts  of  the  chick  and 
frog  are  essentially  the  same,  except  for 
the  presence,  in  the  frog,  of  an  extra  pair 
of  arches  and  clefts,  and  of  the  gills  which 
border  the  visceral  arches  of  the  frog,  but 
are  not  present  at  any  stage  in  the  develop- 
ment of  the  chick.  The  presence  in  the  chick 
of  these  fish-like  though,  to  it,  functionless 


192          Vertebrate  Embryology 


structures  is  to  be  explained  only  by  as- 
suming that  the  birds  are  descended  from 
aquatic  and  gill-breathing  animals.  The  frog, 
being  less  distantly  removed  from  the  fish,  or 
fish-like  ancestors,  still  retains  the  gills  in  a 
functional  condition,  during  the  early  part  of 
its  development. 

Although    the     changes     involved    in    the 


FIG.  63. — TRANSVERSE  SECTION  THROUGH  THE  ANTERIOR  PART 
OF  AN  EMBRYO  OF  68  HOURS.  Owing  to  the  curvature  of  the 
embryo  the  section  passes  through  it  twice.  (After  Duval.) 

ABi-^  first  to  fifth  branchial  arches.  AAo^  aortic  arch  of  the  fifth  branchial 
arch.  A0,  aorta.  Ci,  bulbus  arteriosus.  Ch,  notochord.  CM,  medullary  canal. 
CR,  lens,  fb  1-4,  first  to  fourth  visceral  clefts.  GS^  spinal  ganglion.  NO,  optic 
nerve.  Ph.,  pharynx.  7!&,  thyroid  gland,  ^i,  fore-brain.  VCA ,  anterior  cardinal 
vein.  VO)  optic  cup. 


ultimate  fate  of  the   visceral 
do    not   take   place    until    a 
will   be   convenient   briefly   to 
changes    at    this    point,    and 
merely    recall    them    to    mind 
times. 

As  has  been  said,  all  four 
clefts  become   closed,  after  a 


clefts  and  folds 

later    period,    it 

describe   those 

then,    perhaps, 

at    the    proper 

of  the  visceral 
short  time,   so 


Development  of  the  Third  Day    193 

that,  as  far  as  can  be  seen  in  surface  views, 
they  disappear.  The  first,  second,  and  third 
clefts  do,  apparently,  completely  disappear 
and  leave  no  trace  in  the  adult ;  but  the 
most  anterior  cleft,  the  hyomandibular, 
although,  like  the  rest,  closing  at  the  outer 
end,  does  not  close  throughout  its  length, 
and  retains  its  connection  with  the  cavity  of 
the  pharynx.  The  exact  changes  that  now 
take  place  are  somewhat  in  dispute,  but  it 
seems  reasonably  certain  that  the  inner,  un- 
closed portion  of  the  cleft  forms  an  enlarge- 
ment, at  its  outer  end,  which  becomes  the 
tympanic  cavity,  while  the  rest  of  the  cleft 
persists  as  the  Eustachian  tube. 

The  external  auditory  meatus  is  built  up 
as  a  short  tube  on  the  outside  of  the  head, 
opposite  the  position  of  the  tympanic  cavity ; 
it  may  be  partially  formed  by  a  slight  de- 
pression of  the  surface  ectoblast.  The  layer 
of  tissue,  formed  by  the  closure  of  the  outer 
end  of  the  hyomandibular  cleft,  which  lies 
between  the  tympanic  cavity  and  the  external 
auditory  meatus,  becomes  the  tympanic  mem- 
brane. It  is  evidently  composed  of  three 
parts  ;  an  external  layer  of  ectoblast,  from  the 
surface ;  an  inner  layer  of  entoblast,  from 


194          Vertebrate  Embryology 

the  lining  of  the  cleft ;  and  a  middle  layer 
of  mesoblast,  from  the  uncleft  mesoblast  of 
the  neck  region.  During  a  greater  part  of 
fcetal  life  the  tympanic  membrane  is  very 
thick,  and  bears  little  resemblance  to  the 
structure  in  the  adult. 

The  changes  above  described,  like  many 
others  given  in  even  so  brief  an  account  as 
this,  can  be  made  out  only  with  great  diffi- 
culty, so  that  the  student  who  is  just  begin- 
ning the  study  of  embryology  will  generally 
have  to  take  such  statements  for  granted. 

The  fate  of  the  visceral  folds  should,  per- 
haps, be  discussed  in  connection  with  the 
development  of  the  skeleton,  but  it  will  be 
convenient  to  take  up  the  discussion  at  this 
point,  along  with  that  of  the  visceral  clefts, 
with  which  they  are  so  intimately  associated. 

The  last  two  arches,  the  so-called  second 
and  third  arches  or  folds,  apparently  entirely 
disappear  and  leave  no  trace  in  the  adult. 

Parts  of  the  two  arches  in  front  of  these, 
that  is,  the  first  visceral  and  the  hyoid,  be- 
come converted  into  the  hyoid  apparatus  of 
the  adult. 

The  first  arch,  the  mandibular,  is  the  most 
important,  in  regard  to  the  adult  structures 


Development  of  the  Third  Day    195 

that  are  derived  from  it.  The  main  branch 
of  this  arch,  on  each  side,  meets  its  fellow 
of  the  opposite  side  in  the  mid-ventral  line, 
and  fuses  to  form  the  basis  of  the  mandible 
or  lower  jaw  ;  hence  its  name,  the  mandibular 
arch  (Fig.  64,  MN).  From  the  anterior  edge 
of  the  dorsal  end  of  each  half  of  the  man- 
dibular arch  a  small  branch  grows  forward 
and  downward,  during  the  fourth  or  fifth 
day  (Fig.  64,  MX\  towards  a  triangular 
median  process  from  the  front  of  the  head. 
This  median  process  has  already  been  men- 
tioned, and  is  named,  from  the  region  of 
the  head  formed  by  it,  \he  fronto-nasal  process 
(Fig.  64,  FP\  The  branches  or  processes 
from  the  mandibular  arch  are  the  maxillary 
processes,  and  from  them  the  upper  half  of  the 
jaw  is  formed.  The  two  maxillary  processes 
do  not  meet  each  other  in  the  middle  line, 
as  do  the  two  parts  of  the  mandibular  arch, 
but  fuse  with  each  side  of  the  median  fronto- 
nasal  process,  to  form  the  upper  half  of  the 
jaws. 

The  abnormality  known  as  harelip,  some- 
times seen  in  human  beings,  is  caused  by 
the  failure  of  one  of  the  maxillary  processes 
to  fuse  completely  with  the  fronto-nasal 


196  Vertebrate  Embryology 

process.  The  space  between  the  mandibu- 
lar  arch  behind,  and  the  fronto-nasal  and 
maxillary  processes  in  front,  will  be  the 
mouth  of  the  chick 


_.{-.  \  !•!  /OK 


oc 


BR 


FIG.  64.  —  THE  HEAD  OF  AN  EMBRYO  CHICK  AT  THE  END 
OF  THE  FIFTH  DAY  OF  INCUBATION  ;  SEEN  FROM  BELOW. 
(After  Marshall.)  Compare  Fig.  72,  A,  for  a  side  view  of 
an  embryo  of  about  the  same  age. 

BR,  first  branchial  arch.  £S,  cerebral  hemispheres.  Cff,  noto- 
chord.  DS,  mouth.  FP,  fronto-nasal  process.  HM,  hyomandibular 
cleft.  HY,  hyoid  arch.  MN,  mandibular  arch.  MX,  maxillary 
arch.  NS,  spinal  cord,  seen  in  section  where  the  neck  has  been  cut 
across.  OC,  eye.  Off,  choroid  fissure.  OK,  olfactory  pit.  OL,  lens. 

The  relation  of  the  parts,  just  described, 
to  each  other  may,  perhaps,  be  made  more 
clear  in  the  following  way  :  —  with  the  hands 
in  front  of  the  body,  and  pointing  down- 
wards, bring  the  tips  of  the  fingers  together, 
the  fingers  of  each  hand  being  slightly  sepa- 


Development  of  the  Third  Day    197 

rated.  The  thumbs  should,  at  first,  be  closely 
pressed  against  the  forefingers,  and  should  be 
considered  as  fused  with  them.  If  the  fingers 
and  hands  are  slightly  bent,  there  will  be  a 
space  between  the  two  hands  that  may  be 
taken  to  represent  the  pharnyx  of  the  chick, 
while  the  four  fingers  will  represent  the  first 
four  gill  arches,  and  the  spaces  between  the 
fingers  will  represent  the  first  three  gill  clefts. 
The  closure  of  the  visceral  clefts  may  be 
represented  by  bringing  the  fingers  of  each 
hand  together.  The  forefingers,  which  should, 
in  reality,  be  the  only  ones  which  actually 
meet  in  the  mid-ventral  line,  will  represent  the 
mandibular  arch,  forming  the  lower  half  of  the 
mouth.  The  formation  of  the  maxillary  arch, 
by  processes  budded  out  from  the  upper  ends 
of  the  mandibular  arch,  may  be  represented 
by  separating  the  thumbs  from  the  fore- 
fingers, and  pointing  them  towards  each 
other,  without  letting  them  come  in  con- 
tact ;  the  triangular  space  between  the  thumbs, 
thus  held,  being  filled,  in  the  imagination,  by 
the  fronto-nasal  process.  The  angles  between 
the  thumbs  and  the  forefingers  will  repre- 
sent the  angles  of  the  mouth.  Of  course,  to 
make  the  comparison  more  striking,  there 


Vertebrate  Embryology 

should  be  one  more  finger,  to  represent  the 
hindermost  arch  and  cleft,  but  as  the  hinder 
arches  and  clefts  form  no  part  of  the  adult 
chick,  this  omission  is  of  little  consequence. 

Further  details  in  the  building  up  of  the 
face  and  head  will  be  given  later. 

The  vascular  system.  By  the  end  of  the 
second  day,  as  has  already  been  said,  there 
are  two  or  three  pairs  of  aortic  arches  present, 
which  carry  the  blood  from  the  bulbus  arte 
riosus  around  the  pharynx  to  the  dorsal  aorta. 

When,  on  the  third  day,  the  visceral  folds 
and  clefts  become  established,  they  bear  a 
very  definite  relation  to  the  aortic  arches.  The 
first  aortic  arch  lies  in  the  first  or  mandibular 
fold ;  the  second  arch  lies  in  the  second  or 
hyoid  fold  ;  the  third  arch  in  the  third  fold, 
etc.;  each  arch  lies  in  its  corresponding  fold 
(Fig.  63,  AB\  and  is  separated  from  the  ad- 
jacent arches  by  the  visceral  clefts. 

The  heart,  during  this  day,  becomes  still 
more  twisted,  and  in  cross-sections  of  the 
chick  it  is  seen,  usually,  as  two  large  cavi- 
ties (Fig.  69,  €2,  C$  )  under  the  body  of  the 
dorsal  region.  It  is  relatively  enormously 
large,  and  lies,  as  yet,  entirely  outside  of 
the  body-cavity  (Fig.  57,  C).  The  ventrally 


Development  of  the  Third  Day    199 

projecting  loop,  the  ventricular  portion,  is  be- 
coming more  pointed,  as  the  apex  of  the 
heart,  and  is  separated  by  slight  constrictions 
from  the  auricular  region,  on  the  one  hand, 
and  the  bulbus,  on  the  other.  There  is,  at  this 
time,  no  separation  of  the  heart  into  right  and 
left  sides. 

The  point  at  which  the  two  vitelline  veins 
unite  to  empty  into  the  heart  now  becomes 
pushed  farther  towards  the  tail,  so  that,  in- 
stead of  these  veins  emptying  simultaneously 
into  the  auricular  portion  of  the  heart,  they 
first  unite  to  form  a  large  single  vessel  which 
then  leads  into  the  heart  (Figs.  66  and  76,  VE). 
This  single  vein  which  brings  all  of  the  blood 
from  the  vascular  area  back  to  the  heart,  first 
through  the  two  vitelline  veins,  and  then,  as  the 
right  vein  dwindles  and  disappears,  through 
the  left  vein  only,  is  called  the  meatus  venosus; 
the  portion  nearest  to  the  heart  being  some- 
times called  the  sinus  venosus ;  and  the  part 
farther  from  the  heart  the  ductus  venosus. 

The  dorsal  aorta  now  gives  off  numerous 
branches  (Figs.  65  and  76)  to  various  parts  of 
the  constantly  enlarging  embryo,  and  the 
blood  that  is  carried  away  from  the  heart  by 
these  branches  is  brought  back  chiefly  by  two 


200          Vertebrate  Embryology 

large  veins  on  each  side  of  the  body  (Fig.  66, 
y,  C)  ;  these  are  the  anterior  and  posterior 
cardinal  veins ;  the  anterior  cardinals,  as  the 
name  would  suggest,  bringing  the  blood  back 


LCA.E. 


FIG.  65. — DIAGRAM  OF  THE  ARTERIAL  CIRCULA- 
TION ON  THE  THIRD  DAY.  (After  Foster  and  Bal- 
four.) 

1,  2,  3,  the  first  three  pairs  of  aortic  arches.  A,  the  vessel 
formed  by  the  junction  of  the  three  pairs  of  arches.  A.O., 
dorsal  aorta,  formed  by  the  junction  of  the  two  branches,  A  , 
it  quickly  divides  into  two  branches,  which  pass  down  one  on 
each  side  of  the  notochord.  Of. A.,  vitelline  artery.  E.CA., 
7.C4.,  external  and  internal  carotid  arteries 

to  the  heart  from  head  region,  and  the  pos- 
terior cardinals  bringing  it  back  from  the 
posterior  end  of  the  body.  The  anterior  and 
posterior  cardinal  veins  of  each  side  unite  to 
form  a  common  vein  that  empties,  at  right 
angles,  into  the  sinus  venosus  (Figs.  66,  dc, 


Development  of  the  Third  Day    201 

and  76,  VD)\  this  transverse  vein  is  called  the 
ductus  Cuvieri,  or   Cuvierian  vein. 

In  order  to  understand  fully  the  evolution 
of  the  complex  avian  circulation  from  the 
simple  and  fish-like  circulation  of  the  embry- 
onic chick,  it  is  important  that  each  stage  in 
the  development  should  be  clearly  understood. 
A  brief  description  of  the  course  of  the  circu- 


FIG.  66. — DIAGRAM  OF  THE  VENOUS  CIRCULA- 
TION OF  THE  THIRD  DAY.  (After  Foster  and  Bal- 
four,) 

//i  heart.  /,  jugular  or  anterior  cardinal  vein,  c,  inferior 
or  posterior  cardinal  vein.  Of,  vitelline  vein,  dc,  ductus 
Cuvieri. 

lation  of  the  blood  at  this  period  will,  there- 
fore, be  given. 

The  blood,  on  entering  the  heart,  is  forced, 
by  the  contraction  of  its  walls,  through  this 
much-twisted  but,  as  yet,  undivided  tube,  to 
the  bulbus  arteriosus ;  from  the  bulbus  it 
passes  dorsalward,  around  each  side  of  the 
pharynx,  through  the  three  pairs  of  aortic 
arches  to  the  two  dorsal  aortae  which  lie 


202  Vertebrate  Embryology 

above  the  pharynx,  on  each  side  of,  or  just 
below,  the  notochord.  Through  small  arteries 
that  are  given  off  from  the  first  aortic  arch, 
or  from  the  anterior  ends  of  the  dorsal  aortse 
(Fig.  65,  I.CA,  and  E.CA),  a  small  amount 
of  blood  finds  its  way  into  the  head  of  the 
embryo,  but  the  greater  part  of  the  blood 
passes  posteriorly  through  the  at  first  double 
and  then  single  (Fig.  65)  aorta ;  the  single 
aorta  soon  becomes  double  again,  as  has  been 
previously  described,  and  through  these  two 
posterior  aortse  the  blood  passes  to  the  hinder 
end  of  the  embryo.  Only  a  small  part  of  the 
blood  is  distributed  to  the  hinder  end  of  the 
embryo,  at  this  period,  however,  the  greater 
part  passing  to  the  vascular  area  through  the 
two  large  vitelline  arteries  that  are  given  off, 
one  on  each  side,  from  the  posterior  paired 
aortae  (Fig.  65,  Of.  A}.  The  blood  from  the 
vascular  area  returns,  through  the  vitelline 
veins,  to  the  meatus  venosus,  and  thence  to  the 
auricular  region  of  the  heart.  The  blood  from 
the  anterior  end  of  the  embryo  returns,  by  the 
anterior  cardinal  veins,  to  the  Cuvierian  veins, 
where  it  meets  the  blood  from  the  posterior 
end  of  the  embryo  that  has  been  brought 
forward  to  that  point  by  the  posterior  car- 


Development  of  the  Third  Day    203 

dinal  veins.  Through  the  Cuvierian  veins  or 
ducts  the  blood  passes  into  the  meatus 
venosus  and  thence  into  the  heart. 

The  alimentary  canal. — By  the  rapid  folding 
off  of  the  embryo  from  the  yolk,  during  this 
day,  the  digestive  tract  becomes  enclosed  for 
the  greater  part  of  its  length.  As  a  matter  of 
convenience,  it  is  sometimes  divided  into  three 
regions :  the  anterior  end  that  is  completely 
enclosed,  having  not  only  roof  and  sides,  but 
also  a  floor,  is  known  as  the  fore-gut ;  the 
middle  region  that  is  still  open  to  the  yolk, 
and  consequently  has  roof  and  sides,  but  no 
floor,  is  the  mid-gut;  and  the  posterior  region 
which,  like  the  fore-gut,  is  completely  enclosed, 
is  the  hind-gut. 

As  the  closing  in  of  the  digestive  tract  con- 
tinues, the  fore-  and  hind-guts,  of  course,  in- 
crease in  length  at  the  expense  of  the  mid-gut 
until  the  seventh  day,  when  the  opening  to 
the  yolk  is  reduced  to  such  a  narrow  opening 
that  the  mid-gut  may  be  considered  to  have 
disappeared.  At  the  end  of  the  third  day,  the 
fore-gut  about  corresponds  to  what  will  be  the 
oesophagus  and  stomach  ;  the  hind-gut  will  be 
the  large  intestine ;  and  the  mid-gut  will  form 
the  small  intestine. 


204          Vertebrate  Embryology 

Up  to  this  time  the  alimentary  canal  lies 
very  high  up  in  the  body-cavity,  being  sepa- 
rated from  the  notochord  and  the  aortae  by 
only  a  broad,  thin  layer  of  mesoblast  (Figs.  48, 
Ph  and  70).  During  this  day,  however,  the 
digestive  canal,  for  a  greater  part  of  its 
length,  draws  away  from  the  upper  side  of 
the  body-cavity,  to  which  it  remains  attached 
by  a  constantly  narrowing  band  of  tissue,  the 
mesentery  (Figs.  71  and  73). 

The  mesentery  is  composed  of  mesoblast 
that  is  continuous  with  that  which  surrounds 
the  entoblast  of  the  digestive  canal,  and  this 
mesoblast  consists  of  an  undifferentiated 
middle  layer,  in  which  the  blood  vessels  are 
later  developed,  and  a  superficial  layer  of 
epithelium,  continuous  with  the  epithelial 
lining  of  the  peritoneal  cavity.  In  the  an- 
terior part  of  the  fore-gut  the  withdrawal  of 
the  digestive  tract  from  the  notochord  is  very 
slight,  as  there  is  little  or  no  development 
of  the  mesentery  in  the  region  of  the 
oesophagus. 

The  anterior  end  of  the  cesophageal  region 
is  broadened  out  to  form  the  pharynx,  where 
the  gill  clefts  are  developed,  as  has  been  de- 
scribed. The  hinder  end  of  the  cesophageal 


Development  of  the  Third  Day   205 

region  is  smaller  and  more  nearly  round  in 
cross-section,  and  is  the  oesophagus  proper ; 
its  posterior  limit  is  indicated  by  the  position 
of  the  lungs,  whose  development  will  shortly 
be  described.  The  fore-gut  still  ends  blindly 


FIG.  67. — DIAGRAM  OF  A  PORTION  OF  THE  DI- 
GESTIVE TRACT  OF  A  CHICK  DURING  THE  FOURTH 
DAY.  (After  Gotte,  from  Foster  and  Balfour.) 

The  black  inner  line  represents  the  hypoblast,  the  outer 
shading  the  mesoblast.  /^,  lung  diyerticulum.  St,  stomach. 
/,  two  hepatic  diverticula  with  their  terminations  united  by 
cords  of  hypoblast  cells.  /,  diverticulum  of  pancreas. 

in    front,    as   the    mouth    has    not  yet    been 
formed. 

It  might  here  be  mentioned  that,  during  the 
sixth  day,  the  lumen  of  the  oesophagus  be- 
comes completely  closed  for  the  greater  part 
of  its  length,  and  remains  closed  for  two  or 
three  days.  Mention  has  already  been  made  of 


206          Vertebrate  Embryology 

a  similar  closure  of  the  oesophagus  in  the  frog, 
and  the  same  phenomenon  is  seen  in  other 
animals.  In  the  chick  the  oesophagus  gradu- 
ally reopens,  from  behind  forwards,  at  about 
the  ninth  day.  What  the  significance  of  this 
curious  fact  may  be  is  not  known. 

The  part  of  the  digestive  tract  behind  the 
oesophagus  becomes  dilated,  on  the  third  day, 
to  form  the  beginning  of  the  stomach  (Fig.  67, 
.5V);  and  the  short  space  between  the  pyloric 
end  of  the  stomach  and  the  open  mid-gut  may 
be  recognized  as  the  duodenum  from  the  fact 
that  there  are  seen,  in  this  region,  the  begin- 
nings of  the  liver  and  pancreas.  The  devel- 
opment of  the  latter  two  organs  will  be 
described  a  little  later. 

The  posterior  end  of  the  digestive  tract 
may  be,  for  a  part  of  the  third  day,  connected 
with  the  neural  tube  by  the  narrow  canal 
which  was  described  in  connection  with  the 
frog  (p.  34),  and  was  called  the  neurenteric 
canal.  In  front  of  the  neurenteric  canal  is  seen 
the  beginning  of  the  cloaca,  as  a  small  pitting- 
in  of  the  external  ectoblast  to  meet  the  ento- 
blast.  This  invagination  of  the  ectoblast  is 
known  as  the  proctodceum,  but  it  does  not 
open  into  the  digestive  tract  until  several  days 


Development  of  the  Third  Day    207 

later  (about  the  fifteenth  day)  ;  so  that  the 
digestive  tract  now  ends  blindly  at  each  end. 
The  proctodaeum  in  the  chick  is  very  shallow, 
and  forms  only  the  actual  external  opening  of 
the  cloaca. 

Up  to  the  sixth  day,  the  digestive  tract 
remains  practically  straight ;  but  after  that 
time  it  begins  to  grow  faster  than  the  cavity 
in  which  it  is  contained,  so  that  it  begins  to 
twist  and  form  the  loops  characteristic  of  the 
adult  intestines. 

About  the  sixth  day  the  gizzard  is  formed 
as  a  thick-walled  outgrowth  from  the  end  of 
the  stomach. 

The  lungs. — The  first  trace  of  the  lungs  is 
seen  on  the  third  day  as  two  small,  hollow 
outgrowths  from  the  ventral  side  of  the  oesoph- 
agus near  its  anterior  end  (Fig.  67,  Ig).  At 
the  point  of  origin  of  these  small  pouches, 
the  oesophagus  becomes  laterally  constricted, 
so  that  in  cross-section  it  is  hourglass-shaped 
(Fig.  68).  By  the  meeting  of  the  lateral  con- 
strictions, the  oesophagus  is  divided  into  two 
parts:  the  upper  part,  or  oesophagus  proper,  and 
the  lower  part,  into  which  the  lung  rudiments 
open,  which  will  be  the  trachea.  At  the  an- 
terior limits  of  the  lateral  constrictions  the 


YJ 


FIG.  68.— TRANSVERSE  SECTION  OF  AN  EMBRYO  OF  THE  FOURTH 
DAY,  PASSING  THROUGH  THE  ANTERIOR  PART  OF  THE  LUNG  RUDI- 
MENTS. (After  Duval.) 

Arn^  amnion.  A o,  aorta.  B P,  bud  of  lung.  C 2  and  €3,  heart.  CC,  Cuvier- 
ian  duct.  Cam,  amniotic  cavity.  CO,  chorion.  7/4,  fore-gut.  Vva,  anterior 
branch  of  vitelline  vein.  VJ,  wall  of  umbilical  stalk.  VM,  mesoblast  of  peri- 
cardium. 


208 


Development  of  the  Third  Day    209 

trachea  and  oesophagus  are  continuous,  and  at 
this  point  will  be  the  glottis. 

As  the  two  lung  rudiments  grow  backwards, 
the  mesoblast  gradually  collects  around  them 
as  two  lobes  (Fig.  69,  BP\  and  it  is  from  the 
mesoblast  of  these  lobes  that  the  elastic, 
muscular,  cartilaginous  and  other  tissues  of 
the  lungs  and  bronchial  tubes  are  formed.  The 
epithelial  lining  of  the  lungs,  down  to  the 
smallest  air-cells,  is  formed  by  the  continuous 
branching  of  the  two  original  entoblastic  out- 
growths from  the  oesophagus  ;  so  that  while 
the  chief  thickness  of  the  walls  of  the  lungs,  as 
well  as  their  blood  vessels,  is  formed  of  meso- 
blast, the  entire  epithelial  lining  is  of  ento- 
blastic origin. 

"  The  air  sacs,  which  are  structures  very  characteris- 
tic of  birds,  appear  about  the  eighth  day  as  thin-walled 
saccular  diverticula  from  the  hinder  edges  of  the  lungs."  ' 

The  liver. — The  origin  of  the  liver,  as  a 
median  outgrowth  from  the  floor  of  the  diges- 
tive tract,  was  briefly  described  in  the  case  of 
the  frog :  its  development  in  the  chick  will  be 
described  more  in  detail. 

"  The  liver  arises,  about  the  middle  of  the  third  day, 
1  Marshall. 


210          Vertebrate  Embryology 

as  a  tubular  diverticulum  from  the  posterior  end  of  the 
fore-gut,  in  the  angle  between  the  two  vitelline  veins, 
and  immediately  behind  their  point  of  union.  A  second 
diverticulum  arises  from  the  same  spot  almost  directly 
afterwards;  it  is  similar  to  the  first,  but  of  rather  smaller 
size.  Both  these  diverticula  have  hypoblastic  walls, 
with  thin  mesoblastic  investments  (Fig.  67,  /). 

"  Towards  the  latter  part  of  the  third  day,  as  the  fold- 
ing off  of  the  embryo  from  the  yolk-sac  proceeds,  the 
liver  diverticula  are  found  to  arise  definitely  from  the 
part  of  the  mesenteron  which  will  later  become  the  duo- 
denum. At  the  same  time  they  come  into  very  close 
relation  with  a  very  large  median  vein,  the  meatus  veno- 
sus,  which  is  formed  by  the  union  of  the  right  and  left 
vitelline  veins  behind  the  heart  (Fig.  76,  VE). 

"  The  two  liver  diverticula  lie  one  on  each  side  of  the 
meatus  venosus,  and  in  very  close  contact  with  this. 
The  hypoblastic  cells  forming  the  walls  of  the  diver- 
ticula now  begin  to  proliferate  freely,  growing  out  as 
solid  strands  of  cells,  which  form  an  irregular  reticulum 
closely  surrounding  the  meatus  venosus;  the  meshes  of 
the  reticulum  being  occupied  by  capillary  blood  ves- 
sels, which  develop  in  the  mesoblast,  and  early  acquire 
connection  with  the  meatus  venosus  itself.  These  pro- 
cesses proceed  rapidlf" during  the  fourth  and  fifth  days, 
and  by  the  end  of  the  fifth  day  (Figs.  76  and  83)  the 
liver  is  an  organ  of  considerable  size,  consisting  of  a 
network  of  solid  rods  of  hypoblast  cells,  which  branch 
and  anastomose  freely  in  all  directions  ;  the  meshes  of 
the  network  being  occupied  by  blood-vessels,  which 
penetrate  all  parts  of  the  liver,  and  are  in  free  com- 
munication with  the  meatus  venosus,  round  which  the 
liver  is  formed. 


Development  of  the  Third  Day    211 

"  The  liver  continues  to  grow  rapidly,  and  by  the 
tenth  day  is  the  largest  organ  in  the  abdominal  cavity. 
The  trabecular  network  of  hypoblast  cells  becomes 
the  liver  parenchyma  ;  the  tubular  diverticula  from  the 
duodenum  branch  out  freely  in  the  substance  of  the 
liver,  and  become  the  two  bile  ducts  of  the  adult  bird  ; 
while  the  gall  bladder  arises  on  the  fifth  day  as  a  sac- 
cular  outgrowth  from  the  right  or  larger  of  the  two 
primary  diverticula. 

"The  early  formation  of  the  liver  in  the  chick,  and 
its  large  size  during  the  greater  part  of  the  develop- 
mental history,  indicate  that  it  must  be  of  considerable 
functional  importance  during  embryonic  life.  Its  rela.- 
tion  to  the  blood  system,  and  especially  the  fact  that  it 
intercepts  the  blood  returning  from  the  yolk-sac  to  the 
heart,  suggest  that  its  chief  purpose  is  connected  with 
the  elaboration  of  food  material  which  is  obtained  from 
the  yolk-sac,  and  at  the  expense  of  which  the  nutrition 
of  the  embryo  is  effected."  1 

The  pancreas  arises  a  little  later  than  the 
liver,  as  a  tubular  diverticulum  from  the  in- 
testine just  back  of  the  liver  (Fig.  67,  /).  A 
second  diverticulum  is  formed  at  about  the 
eighth  day,  and,  still  later,  a  third  appears. 
These  diverticula  persist  as  the  three  pancre- 
atic ducts  of  the  adult,  but  the  lobes  with 
which  they  are  connected  fuse  together. 

The   thyroid  body. — At    the    close    of    the 

1  Marshall. 


212  Vertebrate  Embryology 

second  day  the  thyroid  body  originates  as 
a  pit  from  the  floor  of  the  pharynx,  opposite 
the  first  pair  of  visceral  arches  (Fig.  63,  Th). 
This  pit  deepens  and  elongates,  and  gradually 
closes  up,  by  the  fusion  of  its  sides,  to  form  a 
solid  rod  of  entoblast  lying  in  a  longitudinal 
position  under  the  floor  of  the  pharynx,  just 
in  front  of  the  truncus  arteriosus.  By  the 
sixth  day,  it  separates  from  the  pharynx,  and 
lies  freely  in  the  mesoblast  of  that  region.  It 
now  becomes  bilobed,  and  the  lobes  send  out 
solid  rods  of  tissue,  which  become  hollowed 
out  to  form  the  vesicles  of  the  adult  thyroid. 
The  thyroid  gradually  shifts  its  position  back- 
wards, and  becomes  surrounded  with  a  sheath 
of  vascular  connective  tissue. 

Changes  in  the  mesoblast. — If  a  tranverse 
section  through  the  middle  region  of  a  second- 
day  chick  be  compared  with  a  similar  section 
of  a  chick  at  the  end  of  the  third  day,  a 
marked  difference  in  the  depth,  in  a  dorso- 
ventral  direction,  will  be  seen  (Figs.  70  and 
71).  This  increase  in  depth  is  due  to  three 
chief  causes :  to  the  greater  slope  of  the  sides, 
on  account  of  the  formation  of  the  side  folds; 
to  the  increase  in  the  mesoblast  between  the 
notochord  and  the  digestive  tract ;  and  to  the 


GN 


Ai 


CO 


FIG.  69. — TRANSVERSE  SECTION  OF  AN  EMBRYO  OF  THE  FOURTH 

DAY,  JUST  POSTERIOR  TO  THE  PRECEDING.       (After  Duval.) 

CH,  notochord.    GN,  nerve  ganglion.    MM,  muscle  plate.    VB,  liver.    Other 
lettering  as  in  Fig.  68. 


213 


2t4          Vertebrate  Embryology 

changes  that  take  place  in  the  mesoblastic 
somites. 

The  formation  of  the  mesoblastic  somites 
has  already  been  described,  and  it  will  be 
remembered  that,  at  the  end  of  the  second 
day,  they  were  more  or  less  triangular  masses 
of  tissue,  frequently  with  a  small  central 
cavity,  probably  a  continuation  of  the  body- 
cavity.  Each  somite  now  increases  in  depth, 
and  its  cavity,  the  myocoel,  shifts  its  position 
until  it  lies  in  the  upper  part  of  the  somite, 
instead  of  near  the  centre.  Then  the  upper 
part  of  the  somite,  with  the  myocoel,  separates 
from  the  lower  part,  and  forms  what  is  known 
as  the  muscle  plate.  The  muscle  plate  consists 
of  closely  packed  cells,  while  the  lower  part  of 
the  somite  is  made  up  of  loosely  arranged 
cells  of  the  stellate  form  so  characteristic  of 
undifferentiated  mesoblast  (Fig.  48,  mes).  The 
muscle  plates  are,  at  first,  nearly  horizontal, 
with  their  inner  ends  slightly  dorsal  to  their 
outer  ends,  but  they  become  more  and  more 
steeply  inclined  until,  at  the  end  of  the  third 
day,  they  are  almost  vertical  (Fig.  69,  MM). 

The  cells  of  the  ventral  walls  of  the  muscle 
plates  become  converted  into  bands  of  longi- 
tudinal muscle  fibres,  which  bands  remain  di- 


Development  of  the  Third  Day    215 

vided  into  blocks  corresponding  to  the  original 
somites :  thus  in  the  chick  embryo  we  have  a 
metameric  arrangement  of  muscles  similar  to 
the  arrangement  of  the  muscles  in  the  adult 
fish. 

The  outer  end  of  the  muscle  plate  rapidly 


pv 


FIG.  70. — TRANSVERSE  SECTION  THROUGH  THE  DORSAL 

REGION  OF  AN  EMBRYO  OF  68  HOURS.       (After  Duval.) 

Am,  amnion.  Ao,  aorta,  hi  and  z'#,  hypoblast.  CM,  neural 
canal.  CW*  Wolffian  duct.  CSW,  nephrostome,  or  segmental  canal 
of  Wolffian  body.  G7,  alimentary  canal.  PV,  muscle  plate.  VCP, 
posterior  cardinal  vein.  VJ,  wall  of  umbilical  stalk. 

extends  into  the  somatopleure,  or  body-wall, 
and  becomes  largely  converted  into  muscle 
fibres  from  which  the  muscles  of  the  back  and 
trunk  are  formed.  The  median  portion  of  the 
mesoblastic  somite,  left  after  the  formation 
of  the  muscle  plates,  is  converted,  as  will  be 
described  later,  chiefly  into  the  vertebrae.  The 


2i6          Vertebrate  Embryology 

origin  of  the  muscles  of  the  appendages  is 
independent  of  the  muscle  plates. 

The  Wolffian  body. — During  the  third  day, 
the  mass  of  mesoblast  between  the  meso- 
blastic  somites  and  the  point  of  divergence 
of  the  somatopleure  and  the  splanchnopleure, 
the  intermediate  cell-mass,  becomes  very 
prominent,  and  is  covered  with  a  sharply 
defined  layer  of  epithelial  cells  (Fig.  54). 
The  intermediate  cell-mass  is  of  importance 
because  from  it,  or  in  it,  are  developed  the 
urinary  and  reproductive  organs.  The  de- 
velopment of  the  Wolffian  duct  has  already 
been  described.  The  origin  of  the  Wolffian 
body,  or  embryonic  kidney,  of  the  chick  will 
now  be  briefly  outlined. 

It  will  be  recalled  that,  in  the  frog,  the 
embryonic  or  temporary  excretory  organ  was 
the  head-kidney  or  pronephros ;  and  that,  as 
the  Wolffian  body  or  permanent  kidney  was 
developed,  the  pronephros  gradually  disap- 
peared. In  the  chick,  the  embryonic  kidney 
is  the  mesonephros  or  Wolffian  body,  and  this 
ceases  to  function  as  an  excretory  organ  shortly 
after  hatching,  and  is  replaced,  in  that  capacity, 
by  the  metanephros  or  permanent  kidney. 
The  pronephros,  in  the  chick,  is  an  extremely 


Development  of  the  Third  Day    2 1 7 

rudimentary  structure,  appearing  after  the 
formation  of  the  Wolffian  body,  and  disap- 
pearing again  almost  immediately. 

There  are,  then,  three  pairs  of  excretory 
organs  in  the  chick  :  the  pronephros  or  head 
kidney,  which  never  functions  as  a  kidney, 
and  which  almost  completely  disappears  very 
early  in  embryonic  life ;  the  mesonephros  or 
Wolffian  body,  which  develops  sooner  than 
the  pronephros,  attains  a  large  size,  and  func- 
tions as  the  kidney  during  embryonic  life  ;  and 
the  metanephros  or  permanent  kidney,  which 
begins  to  develop  quite  early,  but  does  not 
become  functional  until  after  hatching. 

The  Wolffian  body  extends  for  the  greater 
part  of  the  dorsal  region  of  the  embryo  chick, 
as  far  back  as  about  the  thirteenth  somite 
(Fig.  74).  In  its  fully  developed  condition 
it  consists  of  a  mass  of  convoluted  tubules, 
opening,  at  one  end,  into  the  Wolffian  duct, 
and  expanded,  at  the  other  end,  into  a  Mal- 
pighian  body.  The  tubules  of  the  anterior 
and  posterior  ends  of  the  Wolffian  body 
have  different  methods  of  development,  and 
hence  must  be  described  separately.  That 
part  of  the  Wolffian  body  which  lies  anterior 
to  about  the  sixteenth  somite  begins  as  a  series 


218          Vertebrate  Embryology 

of  small  pits  or  nephrostomes  pushing  into  the 
mesoblast  from  the  body-cavity,  a  little  below 
and  to  the  median  side  of  the  Wolffian  duct 
(Fig.  54,  CWS}.  Between  the  bottoms  of 
these  little  nephrostomes  and  the  Wolffian 
duct  small  twisted  rods  of  cells  appear  which 
soon  become  hollow,  and  open  into  the  Wolf- 
fian duct,  at  one  end,  and  into  the  nephros- 
tomes at  the  other.  Thus,  through  these 
Wolffian  tubules,  the  body  cavity  is  brought 
into  communication  with  the  Wolffian  duct. 
These  tubules  soon  degenerate,  and  nearly  all 
of  them  disappear  completely. 

The  Wolffian  tubules  of  that  part  of  the 
Wolffian  body  that  lies  back  of  the  sixteenth 
somite  do  not  open  into  the  body-cavity :  that 
is,  there  are  no  nephrostomes.  The  tubules 
of  this  region  begin  as  small  vesicles  in  the 
mesoblast  between  the  Wolffian  duct  and  the 
body  cavity.  These  vesicles  become  elon- 
gated to  form  the  tubules,  and,  at  their  inner 
ends,  acquire  connection  with  the  cavity  of 
the  Wolffian  duct,  while  their  outer  ends 
become  enlarged  to  form  the  Malpighian 
bodies.  By  the  increase  in  the  number  of 
the  tubules,  and  by  the  increase  in  the  length 
of  each  tubule,  causing  it  to  become  greatly 


Development  of  the  Third  Day    219 

twisted  and  convoluted,  the  Wolffian  body 
becomes  greatly  enlarged,  and  causes  the 
marked  ridge  that  projects  into  the  body- 
cavity  on  each  side  of  the  median  line  (Fig.  71). 
Owing  to  the  above-described  changes  that 


YOM 


FIG.  71. — TRANSVERSE  SECTION  THROUGH  THE  DORSAL 
REGION  OF  AN  EMBRYO  OF  68  HOURS,  A  SHORT  DISTANCE 

ANTERIOR    TO     THAT     REPRESENTED     IN    FlG.     70.       (After 

Duval.) 

Cam,  amnioric   cavity.     VOM  and  Vvl,  vitelline  veins.     Other 
lettering  as  in  Fig.  70. 

have  taken  place  in  the  mesoblast  of  the 
trunk,  the  position  of  the  Wolffian  duct  is 
changed,  during  this  day.  Instead  of  lying 
close  under  the  ectoblast  as  it  did  during  the 
second  day  (Fig.  54,  CW),  it  shifts  its  position 
downwards  until  it  lies  near  the  middle  of  the 


220          Vertebrate  Embryology 

intermediate  cell-mass,  and  may  even  project, 
somewhat,  into  the  body-cavity  (Fig.  71,  CIV). 

The  final  fate  of  the  Wolffian  body,  as  well 
as  the  development  of  the  pronephros  and  the 
metanephros,  will  be  taken  up  later. 

Summary  of  the  third  day  : 

1.  Turning  of  the  embryo  to  lie  on  its  left 
side. 

2.  Increase  of   cranial   flexure,    and   begin- 
ning of  body  flexure. 

3.  The  formation  of  the  four  gill  clefts  and 
the  five  gill  arches. 

4.  The  completion  of  the  circulation  of  the 
vascular    area ;    the    increased    curvature    of 
the  heart,  and  the   indication  of   its   division 
into  chambers  ;  the  appearance  of  new  aortic 
arches,  of  the  cardinal  veins,  and  of  the  meatus 
venosus. 

5.  The  formation  of  the  optic  cup. 

6.  The  formation  of  the  lens  vesicle. 

7.  The  formation  of  the  nasal  pits. 

8.  The   closing  in  of  the  auditory  vesicles. 

9.  The  first  indication  of  the  cerebral  hem- 
ispheres, and  the  separation  of  the  hind-brain 
into  cerebellum  and  medulla  oblongata. 

10.  The  definite   establishment  of  the  cra- 
nial and  spinal  nerves. 


Development  of  the  Third  Day    221 

11.  The    formation     of     the    fore-gut    and 
hind-gut ;  and  the    separation    of    the    former 
into  oesophagus,  stomach,  and  duodenum,  and 
of  the  latter  into  large  intestine  and  cloaca. 

12.  The    formation   of  the  lungs  as  diver- 
ticula   from    the    oesophagus  just    anterior  to 
where  it  enlarges  to  form  the  stomach. 

13.  The    formation   of    the    liver  and    pan- 
creas as  diverticula  from  the  duodenum,  just 
posterior  to  the  stomach. 

14.  Formation    of   the   muscle   plates;  and 
other  mesoblastic  changes. 

15.  Definite    formation    of     the     Wolffian 
bodies. 

1 6.  Growth  of  the  allantois. 

1 7.  The  completion  of  the  amnion. 


CHAPTER  VI 

THE   DEVELOPMENT  OF  THE   FOURTH   DAY 

ON  opening  an  egg  at  the  end  of  the  fourth 
day  of  incubation  (Fig.  72),  one  is 
struck  with  the  increase  in  size  of  the 
embryo,  which  now,  on  account  of  the  rapid 
absorption  of  the  white  of  the  egg,  lies  so  close 
to  the  shell  that  the  latter  must  be  removed 
with  some  care,  in  order  that  the  embryo  may 
not  be  injured. 

The  germinal  membrane  now  embraces 
about  half  of  the  yolk,  and  the  vascular  area  is 
very  prominent,  though  the  sinus  terminalis 
has  already  begun  to  diminish  in  distinctness. 

The  distinctness  of  the  outlines  of  the  em- 
byro  is  somewhat  obscured  by  the  amnion, 
which  now  forms  a  complete  covering  over 
it.  There  is,  as  yet,  very  little  fluid  in  the 
amniotic  cavity,  so  that  the  inner  amnion 
forms  a  very  close  investment  of  the  embryo 

(Fig.  57). 

The  folding  off  of  the  embryo  has  continued, 

222 


Development  of  the  Fourth  Day    223 

until  now  the  splanchnic  stalk  is  reduced  to 
a  very  narrow  but  distinct  tube,  connecting 
the  yolk-sac  with  the  nearly  enclosed  mid-gut. 
The  somatic  stalk  has  not  progressed  so  far, 
so  that  there  is  a  ring-shaped  space  between  it 
and  the  splanchnic  stalk  :  through  this  space 
projects  the  allantois,  which  is  very  much  in 
evidence  as  a  large,  sac-like  object,  connected 
by  a  narrow  stalk  with  the  hind-gut,  just  in 
front  of  the  well-developed  tail  (Fig.  72,  all). 
The  cranial  flexure  increases  to  such  an  ex- 
tent, during  this  day,  that  the  front  end  of  the 
head  forms  an  acute  angle  with  the  neck  and 

o 

hind-brain  ;  and  by  the  increase  of  the  body 
flexure  as  well,  the  outer  curvature  of  the  em- 
bryo forms  almost  a  semicircle,  and  the  fore- 
brain  and  tail  are  only  a  short  distance  apart 
(Fig.  72). 

The  embryo  continues  to  increase  in  depth 
(compare  Figs.  71  and  73),  and  the  muscle 
plates  are  now  nearly  vertical  in  position,  and 
extend  to  about  the  point  of  separation  of  the 
somatopleure  and  the  splanchnopleure.  Just 
beyond  this  point  of  separation,  the  somato- 
pleure is  elevated  to  form  a  longitudinal  ridge, 
on  each  side,  known  as  the  Wolffian  ridge 
(Fig.  71). 


224          Vertebrate  Embryology 

One  of  the  most  important  and  character- 
istic events  of  this  day  is  the  appearance  of 
the  appendages,  the  wings  and  legs.  They 
are  formed  as  local  swellings  or  thickenings 
of  the  Wolffian  ridge.  Each  limb  consists  of 
a  core  of  compact  mesoblast  covered  with  a 
layer  of  ectoblast.  The  swellings  that  are  to 
form  the  wings  appear  just  back  of  the  region 
of  the  heart,  while  the  legs  are  formed  just  in 
front  of  the  tail  (Fig.  72,  f.l  and  k.l).  The 
limb  buds  are,  at  first,  conical  or  triangular  in 
outline,  but  they  soon  begin  to  differentiate,  so 
that,  by  the  end  of  this  day,  it  may  be  possi- 
ble to  distinguish  between  the  wings  and  legs 
by  their  shape  as  well  as  by  their  position  ; 
the  wings  being  comparatively  long  and  nar- 
row, while  the  legs  are  short  and  broad. 

The  head. — The  cerebral  hemispheres  (Fig. 
51,  VH}  are  becoming  very  large  compared 
with  the  thalamencephalon,  Vi,  from  which  they 
sprang ;  and  the  separation  of  the  cerebellum 
from  the  medulla  is  becoming  more  marked. 
The  mid-brain  is  now  relatively  larger  than  at 
any  other  time,  and  forms  the  large  rounded 
protuberance  at  the  angle  of  the  cranial 
flexure  (Fig.  72,  m.br).  The  eyes  are  enor- 
mously large,  compared  with  the  size  of  the 


Development  of  the  Fourth  Day    225 

embryo,  and  project  strongly  from  the  sides 
of  the  head.  The  mesoblast  surrounding  the 
brain  is  increasing  in  amount,  and  is  begin- 
ning to  show  slight  indications  of  the  forma- 


FlG.  72. — TWO  STAGES  IN  THE  DEVELOPMENT  OF  THE  CHICK 
EMBRYO.  A,  AT  ABOUT  THE  FIFTH  DAY  OF  INCUBATION  ;  B,  AT 
ABOUT  THE  NINTH  DAY  OF  INCUBATION.  IN  A  THE  AMNION  HAS 
BEEN  ALMOST  ENTIRELY  REMOVED,  AND  IN  B  ALL  OF  THE  FCETAL 
APPENDAGES,  EXCEPT  A  SMALL  PART  OF  THE  UMBILICAL  STALK,  HAVE 

BEEN  REMOVED.     (After  Parker  and  Haswell,  from  Duval.) 

all,  allantois.  am,  cut  edge  of  amnion.  an,  anus,  au.afi,  auditory  aperture. 
au.s,  auditory  sac.  f.br,  fore-brain.  _/"/,  fore-limb,  h.br,  hind-brain,  h.l,  hind- 
limb,  ht,  heart,  hy,  hyoid  arch,  m.b,  mid-brain,  mn,  mandibular  arch.  na, 
nostril.  t,  tail. 

tion  of  the  skull.  All  these  changes  begin  to 
give  the  anterior  end  of  the  chick  the  appear- 
ance of  a  distinct  head.  The  fronto-nasal 
process  (page  195)  begins  to  show  promi- 
nently as  an  outgrowth  from  the  fore  part 
15 


226          Vertebrate  Embryology 

of  the  head,  and  the  maxillary  process  of  the 
mandibular  arch  is  also  becoming  well  devel- 
oped (Fig.  64,  MN).  The  nasal  pit  is  deep, 
and  is  connected  with  the  mouth  invagination 
or  stomodaeum  by  the  groove  that  will  form 
the  posterior  nares,  in  the  way  described  on 
page  187.  The  bottom  of  the  stomodaeum 
is  now  separated  from  the  front  end  of  the 
alimentary  canal  by  only  a  thin  partition,  and, 
by  the  end  of  this  day,  this  partition  becomes 
perforated  and  puts  the  stomodseum  into 
communication  with  the  rest  of  the  digestive 
tract.  As  the  mouth  is  formed  by  the  pushing 
in  of  the  ectoblast  in  front  of  the  anterior  end 
of  the  pharynx,  and  by  the  upgrowth  of  the 
parts  surrounding  this  invagination,  it  is 
evident  that  the  buccal  cavity  must  be  lined 
with  ectoblast  instead  of  with  entoblast,  as  is 
the  rest  (except  the  cloaca)  of  the  digestive 
tract  (compare  with  frog,  page  46). 

By  gently  pressing  the  head  of  the  fresh 
embryo  the  cranial  nerves  and  their  ganglia 
may  be  seen,  on  each  side  of  the  auditory 
vesicles. 

The  vertebral  column. — Although  the  forma- 
tion of  the  vertebral  column  does  not  proceed 
very  far  during  this  day,  it  will  be  a  convenient 


Development  of  the  Fourth  Day    227 

place  to  describe  the  entire  development  of 
that  important  structure  in  more  or  less  detail. 

During  the  fourth  day,  the  mesoblastic 
somites  increase  in  number  from  about  thirty 
to  forty,  and  each  somite  has  been  divided,  as 
has  been  explained,  into  an  outer  part,  or 
muscle  plate,  and  an  inner  part  of  less  differ- 
entiated mesoblast  from  which  the  vertebral 
column  will  be  developed,  This  mesoblast 
increases  in  amount,  and  by  sending  out  pro- 
cesses both  above  and  below  the  neural  canal, 
and  also  below  the  notochord,  these  structures 
become  completely  surrounded  by  mesoblast, 
which,  by  the  end  of  the  fourth  day,  has 
acquired  a  considerable  thickness,  and  is  some- 
times known  as  the  membranous  vertebral 
column.  This  membranous  vertebral  column 
still  retains  the  tranverse  lines  of  segmentation 
of  the  original  mesoblastic  somites.  Early  on 
the  fifth  day,  however,  these  lines  of  demarca- 
tion disappear,  and  the  mesoblast  surrounding 
the  neural  canal  and  the  notochord  becomes 
a  continuous  tube.  This  does  not  apply  to 
the  muscle  plates,  which  retain  their  original 
planes  of  segmentation. 

During  the  fifth  day,  the  mesoblast  in  im- 
mediate contact  with  the  notochord  becomes 


228  Vertebrate  Embryology 

cartilaginous,  and  forms  a  continuous  cartilagi- 
nous sheath  around  the  notochord  through- 
out its  entire  length.  At  the  sides  of  the 
spinal  cord  there  are  formed  paired  bars  of 
cartilage,  which  soon  fuse  with  the  cartilagi- 
nous sheath  of  the  notochord,  and  form  the 
rudiments  of  the  neural  arches. 

Before  the  end  of  the  fifth  day,  marked  his- 
tological  changes  take  place  in  the  cartilaginous 
tube  surrounding  the  notochord.  Opposite  the 
points  of  attachment  of  the  neural  arches 
the  cartilage  becomes  more  mature,  while 
in  the  spaces  between  the  arches  it  retains 
its  embryonic  character.  In  this  way  the 
cartilaginous  tube,  though  still  an  unsegmented 
structure,  is  marked  off  into  a  series  of  ver- 
tebral and  intervertebral  rings  ;  the  vertebral 
rings  being  the  parts  to  which  the  neural 
arches  are  attached,  the  intervertebral  rings 
the  parts  between  the  neural  arches. 

About  the  end  of  the  fifth  day,  each  inter- 
vertebral ring  becomes  divided  transversely 
into  two  equal  parts,  and  each  of  these  parts 
attaches  itself  to  the  adjacent  vertebral  ring. 
In  this  way,  the  once  continuous  cartilaginous 
sheath  of  the  notochord  becomes  divided  into 
3.  series  of  segments,  each  segment  consisting 


Development  of  the  Fourth  Day    229 

of  a  vertebral  ring,  with  its  attached  neural 
arch,  and  the  anterior  and  posterior  halves, 
respectively,  of  the  succeeding  and  preceding 
intervertebral  rings.  The  segments  so  formed 
become  the  vertebra  of  the  adult.  The 
planes  of  this  secondary  or  permanent  segmen- 
tation, as  it  is  sometimes  called,  do  not  corre- 
spond with  the  planes  of  segmentation  of  the 
mesoblastic  somites,  or  the  primary  segmen- 
tation. The  secondary  segmentation  takes 
place  in  such  a  way  that  the  lines  of  separation 
between  the  newly  formed  vertebrae  lie  oppo- 
site the  centres  of  the  muscle  plates.  By  this 
alternate  arrangement  of  the  muscle  segments 
and  the  vertebral  segments,  each  vertebra  is 
acted  upon,  on  each  side,  by  two  muscles,  the 
preceding  muscle  being  attached  to  the  an- 
terior half  of  the  vertebra,  the  succeeding 
muscle  to  the  posterior  half.  The  advantage 
of  this  arrangement  in  producing  motion  or 
bending  of  the  spinal  column  is  too  evident  to 
need  explanation. 

Although  the  segmentation  of  the  cartilagi- 
nous tube  that  surrounds  the  notochord  has 
been  called  "  secondary,"  it  is  really  not  sec- 
ondary in  the  strictest  sense  of  the  word. 
This  segmentation  is  concerned  only  with  the 


230          Vertebrate  Embryology 

vertebral  column,  not  with  the  musculature, 
and  before  this  segmentation  takes  place,  the 
vertebral  column  is  represented  by  the  unseg- 
mented  notochord. 

Until  about  the  sixth  or  the  seventh  day,  the 
notochord  is  undiminished  in  size  and  of  nearly 
uniform  diameter  throughout ;  but  after  that 
time  it  is  constricted  and  encroached  on,  at  regu- 
lar intervals,  by  the  growth  inwards  of  the  cen- 
tra of  the  vertebrae,  and  it  finally  disappears, 
though  a  trace  of  it  long  remains,  in  the  inter- 
vertebral  regions,  as  the  ligamenta  suspensoria. 

Ossification  begins  about  the  twelfth  day,  in 
the  centrum  of  the  second  or  the  third  cervical 
vertebra,  and  gradually  extends  backwards. 
The  neural  arches  ossify  a  little  later,  and 
independently  of  the  centra,  each  having  two 
centres  of  ossification. 

About  the  seventh  day,  the  centrum  of  the 
first  cervical  vertebra,  or  atlas,  separates  from 
the  rest  of  the  bony  ring,  and  becomes  at- 
tached to  the  axis,  of  which  it  forms  the  odon- 
toid process. 

In  the  embryo  of  seven  days  there  are 
present  forty-five  vertebrae,  of  which  the  hind- 
ermost  five  or  six  fuse,  at  a  later  period,  to 
form  the  pygostyle. 


Development  of  the  Fourth  Day    231 

The  notochord. — In  connection  with  the 
development  of  the  vertebral  column,  a  few 
words  should  be  said  about  the  changes  that 
take  place  in  the  notochord.  The  origin  of 
the  notochord,  during  the  first  day,  as  a  longi- 
tudinal, rod-like  thickening  of  the  entoblast 
has  been  mentioned.  It  is  at  first  a  solid  rod 


CO 


FIG.  73.— TRANSVERSE  SECTION  THROUGH  THE  DORSAL  REGION 
OF  AN  EMBRYO  OF  96  HOURS.     (After  Duval.) 

Am,  amnion.  Cam,  amnioric  cavity.  CO,  chorion.  7G,  alimentary  canal. 
PPE,  body  cavity  (external).  PPI,  body  cavity  (internal).  VJ,  wall  of  umbilical 
stalk.  VOM,  vitelline  vein. 

of  somewhat  radially  arranged  cells,  but  dur- 
ing the  third  day  some  of  the  central  cells 
become  vacuolated,  their  protoplasm  collecting 
as  a  thin  peripheral  layer,  while  a  clear,  ap- 
parently watery  material,  collects  in  the  centre. 
In  the  peripheral  layer  of  protoplasm  the  nu- 
cleus is  seen. 

Towards  the  end  of  the  third  day,  a  thin 
structureless  sheath  is  formed  around  the 


232  Vertebrate  Embryology 

notochord,  probably  as  a  product  of  the  periph- 
eral cells.  During  the  fourth  day,  all  the 
cells  of  the  notochord  become  vacuolated,  and 
the  vacuoles  continue  to  increase  in  size  until, 
on  the  sixth  day,  they  make  up  almost  the 
entire  cell,  the  protoplasm  being  reduced  to 
an  extremely  thin  wall  around  each  cell ;  the 
nuclei  are  very  indistinct  if  not  quite  invisible. 
Thus  is  the  notochord  converted  into  a  spongy 
network,  the  fine  meshes  of  the  network  being 
the  remains  of  the  walls  of  the  originally  solid 
cells  (Figs.  55,  nek,  73).  The  notochord 
reaches  its  greatest  development  on  the  sixth 
day  ;  and  after  that  time  it  is  gradually  en- 
croached on  by  the  growth  of  the  vertebrae,  as 
has  already  been  described,  until  it  finally 
disappears. 

The  notochord  is  the  most  characteristic 
structure  of  the  great  group  of  animals  known 
as  the  chordata,  being  found  in  all  represen- 
tatives of  this  group,  either  during  the  embry- 
onic period  only,  or  throughout  life.  In  the 
higher  members  of  the  group,  as  in  the  chick, 
it  is  a  very  prominent  and  characteristic  em- 
byronic  structure,  but  disappears  in  the  adult : 
in  some  of  the  lowest  members  of  the  group, 
as  in  the  little  fish-like  Amphioxus,  it  persists 


Development  of  the  Fourth  Day    233 

throughout  life  as  the  animal's  "backbone"  or 
primitive  vertebral  column. 

The  Wolffian  bodies. — By  the  end  of  this 
day,  the  tubules  of  the  anterior  end  of  the 
Wolffian  body  have  disappeared ;  but  the 
tubules  of  the  posterior  end  have  increased 
in  size,  and  become  very  much  convoluted,  so 
that  the  intermediate  cell-mass,  in  which  they 
lie,  projects  still  more  prominently  into  the 
body-cavity.  In  cross-sections  of  the  chick, 
the  convoluted  Wolffian  tubules  are  seen  cut 
across  at  various  angles  :  they  may  usually  be 
distinguished  from  the  Wolffian  duct  by  the 
fact  that  their  walls  are  made  up  of  a  some- 
what thicker  epithelium  than  that  of  the  duct 
(Figs.  73  and  74).  The  glomeruli  of  the 
Malpighian  bodies  are  usually  seen,  in  cross- 
sections,  to  be  filled  with  blood  corpuscles. 

As  has  been  said,  the  Wolffian  body,  or 
mesonephros,  functions  as  the  kidney  during 
the  greater  part  of  the  embryonic  life  of  the 
chick,  but  disappears  before  hatching,  or  at 
least  ceases  to  function,  and  is  replaced  by  the 
permanent  kidneys.  In  most  of  the  fishes  and 
amphibians  the  Wolffian  body  is  the  func- 
tional kidney  throughout  life. 

The  pronephros    and  the  Miillerian  duct. — "  Towards 


234          Vertebrate  Embryology 

the  end  of  the  fourth  day,  three  pit-like  involutions  of 
the  peritoneal  epithelium  appear,  one  behind  another, 
close  to  the  outer  side  of  the  Wolffian  duct,  and  three  or 
four  somites  behind  its  anterior  end  (Fig.  74,  M).  A 
ridge-like  thickening  of  the  peritoneal  epithelium  con- 
nects the  three  pits  of  each  side  with  one  another,  and 
grows  backwards  behind  the  third  pit  as  a  solid  rod  of 
cells,  lying  along  the  outer  side  of  the  Wolffian  duct,  and 
very  close  to  this.  This  rod  soon  becomes  tubular, 
ending  blindly  behind,  but  opening  in  front  into  the 
body  cavity  through  the  three  pits.  These  three  pits 
form  the  head-kidney  of  the  chicken  embryo,  and  the  tube 
into  which  they  open  is  the  commencement  of  the 
Mullerian  duct.  Towards  the  end  of  the  fifth  day  the 
two  hinder  pits  close  up  and  disappear.  The  anterior 
pit  persists,  and  forms  the  peritoneal  opening  of  the 
Mullerian  duct  or  oviduct.  The  Mullerian  duct  itself 
grows  rapidly  backwards  ;  it  lies  in  close  contact  with 
the  outer  wall  of  the  Wolffian  duct,  and  in  its  hinder 
part  appears  to  be  formed  from  cells  derived  from  the 
wall  of  the  Wolffian  duct.  About  the  end  of  the  sixth 
day,  the  Mullerian  duct  has  grown  backwards  as  far  as 
the  cloaca.  It  remains  blind  at  its  hinder  end  in  the 
male,  but  in  the  female  opens,  at  a  later  stage,  into  the 
cloaca"  1 

and  becomes  the  oviduct.  It  is  only  on  the  left 
side  of  the  female,  however,  that  the  Muller- 
ian duct  becomes  the  oviduct :  on  the  right 
side  it  practically  disappears,  though  a  trace 
of  it  may  persist  in  the  adult.  In  the  male 

1  Marshall. 


Development  of  the  Fourth  Day    235 

both  Mullerian  ducts  degenerate  and  become 
almost  completely  obliterated. 

The  metanephros  or  permanent  kidney. — The 
permanent  kidneys  begin  to  develop  towards 
the  end  of  the  fourth  day,  in  the  mesoblast 
between  the  hinder  end  of  the  Wolffian  body 
and  the  cloaca.  The  posterior  end  of  the 
Wolffian  body  is  in  the  thirtieth  somite,  while 
the  cloacal  opening  of  the  Wolffian  duct  is 
opposite  the  thirty-fourth  somite,  so  that 
there  is  a  space  of  three  or  four  somites  be- 
tween the  two  points  ;  it  is  in  this  space  that 
the  first  trace  of  the  permanent  kidney  appears. 

Like  the  mesonephros,  the  first  part  of  the 
metanephros  to  be  formed  is  its  duct,  the 
ureter.  The  ureter  is  formed  as  an  anteriorly 
directed  diverticulum  from  the  dorsal  side  of 
the  posterior  end  of  the  Wolffian  duct.  It 
grows  forwards  on  the  outer  side  of  the  mass 
of  mesoblast  that  lies  behind  the  Wolffian 
body,  and,  for  a  time,  opens,  as  is  evident 
from  its  method  of  formation,  into  the  hinder 
end  of  the  Wolffian  duct :  but  on  the  sixth 
day  it  acquires  a  separate  opening  into  the 
cloaca.  From  the  ureter  lateral  outgrowths 
arise,  and  these,  becoming  connected  with 
rods  of  tissue  in  the  surrounding  mesoblast, 


236          Vertebrate  Embryology 

form  the  tubules  and  Malpighian  bodies  of  the 
permanent  kidney,  very  much  in  the  same  way 
that  the  tubules  of  the  Wolffian  body  were 
formed. 

The  metanephros  is  very  small,  compared  to 
the  Wolffian  body,  during  a  large  part  of  the 
period  of  incubation  ;  but  shortly  before  hatch- 
ing, it  increases  rapidly  in  size,  and  grows  for- 
wards, dorsal  to  the  Wolffian  body.  Before 
describing  the  origin  of  the  reproductive 
organs  proper,  the  ovaries  and  testes,  it  will 
be  well  to  recapitulate  briefly  the  changes 
undergone  by  the  urinary  organs  in  changing 
from  the  embryonic  to  the  adult  condition. 

The  Wolffian  body,  in  the  male,  almost 
entirely  disappears,  but  a  small  portion  of  it 
persists  in  the  adult,  chiefly  as  the  epididymis. 
In  the  female  a  very  small  portion  of  the 
Wolffian  body  persists  in  the  adult,  as  the 
parovariiim,  a  body  that  lies  in  the  mesentery 
between  the  ovary  and  the  kidney.  The 
Wolffian  duct  persists  in  the  male  as  the 
vas  deferens :  in  the  female  it  disappears. 

The  head-kidney  or  pronephros  is,  in  both 
sexes,  a  very  rudimentary  and  transient  struct- 
ure, and  leaves  no  trace  in  the  adult. 

The  Mullerian  duct  never  opens   into  the 


Development  of  the  Fourth  Day    237 

cloaca  in  the  male,  and  almost  completely  dis- 
appears in  the  adult.  In  the  female,  the  right 
Mullerian  duct  becomes  rudimentary,  while 
the  left  duct  becomes  enlarged  to  form  the 
oviduct,  its  peritoneal  opening  persisting  as 
the  funnel-like  opening  of  the  adult  oviduct. 

The  ureter  in  the  adult  of  both  sexes  is 
formed  as  a  narrow  anteriorly  directed  diver- 
ticulum  from  the  posterior  end  of  the  Wolffian 
duct. 

The  reproductive  organs. — The  collection  of 
cells  lying  at  the  upper  angle  of  the  body- 
cavity  and  somewhat  below  and  to  the  out- 
side of  the  aorta  (Fig.  73)  has  already  been 
spoken  of  as  the  intermediate  cell-mass ;  and 
it  has  been  mentioned  that  by  the  fourth 
day  this  intermediate  cell-mass  projects,  as 
a  rounded  ridge,  into  the  upper  part  of 
the  body-cavity,  and  may  be  now  called  the 
genital  ridge,  or  Wolffian  ridge.  The  term 
"  genital  ridge  "  is  applied,  by  some  workers, 
to  the  whole  ridge  that  fills  the  upper  angle  of 
the  body-cavity  on  each  side :  other  authors  use 
the  term  "  Wolffian  ridge  "  for  the  entire  ridge, 
and  restrict  the  term  genital  ridge  to  the  inner 
part  of  the  large  ridge,  next  to  the  splanch- 
nopleure,  where  the  reproductive  organs  are 


238  Vertebrate  Embryology 

actually  formed.  We  shall  use  the  term  "  Wolff- 
ian  ridge"  for  the  entire  mass  of  mesoblast  that 
projects  into  the  upper  part  of  the  body-cavity, 
and  that  forms  the  externally  visible  ridge 
that  has  already  been  spoken  of  as  the  Wolff- 
ian  ridge  (page  223). 

The  whole  Wolffian  ridge  is  for  a  time 
covered  evenly  with  a  single  layer  of  columnar 
epithelium,  which  may  even  extend,  for  a  short 
distance,  over  the  adjacent  parts  of  the  so- 
matopleure  and  splanchnopleure  (Fig.  70). 
The  central  part  of  the  Wolffian  ridge  is 
occupied  by  the  Wolffian  body  and  duct,  and 
it  is,  in  fact,  the  increase  in  size  of  the  former 
that  is  the  chief  cause  of  the  increase  in  prom- 
inence of  the  Wolffian  ridge  (Fig.  74).  The 
epithelial  cells  covering  this  middle  portion  of 
the  ridge  rapidly  lose  their  columnar  character 
and  become  flattened.  The  cells  of  the  outer 
part  of  the  ridge,  next  to  the  somatopleure, 
retain  for  a  longer  time  their  columnar  char- 
acter, and  it  is  here  that  the  involution  to 
form  the  Mullerian  duct  takes  place. 

At  the  inner  angle  of  the  Wolffian  ridge, 
next  to  the  splanchnopleure,  the  columnar  cells, 
instead  of  diminishing  in  distinctness,  become 
more  distinct,  and  even  become  several  layers 


Development  of  the  Fourth  Day    239 

in  depth.  At  the  same  time  the  mesoblast  of 
that  region  becomes  thickened  to  form  a  dense 
area  under  the  epithelial  cells  (Fig  74,  EE). 
This  is  the  true  genital  ridge  or  sexual  emi- 
nence, from  which  the  ovary  or  testis  will  be 
formed. 

Certain  of  the  cells  of  the  germinal  epithe- 


" 


FIG.  74.  —  TRANSVERSE  SECTION  THROUGH  THE 
WOLFFIAN  BODY.     (After  Duval.) 

Ac,  aorta.  CSW,  segmental  tube.  EE,  germinal  epi- 
thelium. 67,  glomeruli.  M,  Mullerian  duct.  WC,  Wolffian 
duct. 

(The  position  of  the  Mullerian  duct  (M)  is  apparently 
wrongly  indicated  in  this  figure.  It  should  be  on  the  outer 
side  of  the  Wolffian  duct.) 

Hum  soon  become  distinguishable  from  the 
rest,  on  account  of  their  greater  size,  more 
rounded  outline,  and  large  nuclei.  These  con- 
spicuous cells,  which  have  a  common  origin 
with  the  other  epithelial  cells  of  the  genital 
ridge,  are  the  primitive  germ  cells  or  gonoblasts 

(Fig-  74)- 

Up  to  this  stage  the    development   is   the 


240          Vertebrate  Embryology 

same  in  all  embryos,  whether  male  or  female, 
and  it  is  not  at  first  possible  to  say  whether 
the  embryo  will  develop  into  a  male  or  into  a 
female. 

In  the  female  the  epithelium  increases 
enormously  in  thickness,  and  the  cells  of  the 
thickened  patch  of  mesoblast  under  it  increase 
in  numbers  to  form  the  stroma  of  the  ovary. 
The  primitive  ova  increase  in  size,  and  the 
smaller  cells  of  the  epithelium  arrange  them- 
selves around  each  ovum  as  a  sort  of  capsule, 
the  follicular  epithelium.  Some  of  the  ova 
sink  down  into  the  underlying  mesoblast,  which 
also  sends  processes  up  into  the  epithelium, 
and  each  ovum  becomes  surrounded  by  a  vas- 
cular sheath  of  connective  tissue  ;  the  ovum 
with  its  follicular  epithelium  and  vascular 
sheath  now  constitutes  a  Graafian  follicle. 

It  is  only  on  the  left  side  that  the  above- 
described  changes  take  place  :  the  ovary  on 
the  right  side  of  the  chick  remains  in  a  rudi- 
mentary condition  throughout  life,  or  may 
disappear  entirely. 

The  development  of  the  testis  is  not  so 
easily  determined  as  that  of  the  ovary.  From 
the  first,  it  is  more  closely  associated  with  the 
Wolffian  body.  As  the  epithelium  thickens, 


Development  of  the  Fourth  Day    241 

it  forms  into  rod-shaped  masses  which  are 
separated  by  septa  of  mesoblast  derived  from 
the  patch  of  thickened  mesoblast  underneath. 
These  rods  of  epithelial  cells  probably  become 
converted  into  the  seminiferous  tubules, 
though  the  exact  way  in  which  this  occurs  is 
not  clearly  understood.  The  development  of 
the  spermatozoa  (spermatogenesis)  from  the 
cells  of  the  seminiferous  tubules  will  be  found 
described  in  larger  books  of  embryology,  or 
in  text-books  of  histology. 

The  heart. —  The  heart  undergoes  some 
marked  changes  during  this  day  (Fig.  75). 
The  pointed  loop  which  will  form  the  apex  of 
the  ventricles  still  projects  somewhat  towards 
the  right,  but  it  is  coming  to  point  in  a  more 
ventral  direction.  Well-marked  constrictions 
now  separate  the  ventricles  from  the  auricles, 
on  one  side,  and  from  the  bulbus,  on  the  other 
(Fig.  75).  Although  there  is  no  external  in- 
dication of  its  formation,  there  is  developed, 
during  this  day,  an  incomplete  septum  divid- 
ing the  ventricle  into  two  chambers.  The 
septum  being,  as  yet,  incomplete  the  two 
chambers  of  the  ventricle  communicate  freely 
with  each  other.  The  bulbus  arteriosus  and 
the  auricles  have  increased  in  size,  and  the 

16 


242          Vertebrate  Embryology 

latter  now  lie  nearly  as  far  forward  as  the 
ventricles.  There  is  probably  no  division  of 
the  auricles  into  two  chambers,  though  the 
external  appearance  would  indicate  such  a  di- 
vision. This  appearance  is  due  to  the  great 
development  of  the  auricular  appendages.1 
The  vascular  system. — Since,  by  the  end  of 


C.A 


FIG.  75.— HEART  OF  A  CHICK  ON  THE  FOURTH 
DAY  OF  INCUBATION  VIEWED  FROM  THE  VENTRAL 
SURFACE.  (After  Foster  and  Balfour.) 

La,  left  auricular  appendage.  C,A,  canalis  auricularis.  z>, 
ventricle.  £,  bulbus  arteriosus. 

this  day,  the  vascular  system  reaches  a  state 
of  considerable  complexity,  and  since  its  fur- 
ther development  is  difficult  to  determine  in 
the  laboratory,  it  will  be  the  best  to  give,  at 
this  place,  the  entire  history  of  the  vascular 
system,  from  the  fourth  day  to  the  establish- 
ment of  the  adult  circulation.  The  condition 
of  the  vascular  system  at  the  close  of  the 

1  Marshall  stales  that  the  interauricular  septum  is  formed  on  this 
day. 


Development  of  the  Fourth  Day    243 

third  day  has  already  been  described  (pages 
198-203). 

The  changes  that  take  place  in  the  arterial 
system  will  first  be  described,  and  then  the 
changes  that  occur  in  the  venous  system. 
At  the  close  of  the  third  day,  it  will  be  re- 
membered, three  pairs  of  aortic  arches  had 
been  formed,  from  before  backwards,  lying 
in  the  mandibular,  hyoid  and  first  viscal 
folds. 

During  the  fourth  day,  two  other  pairs  of 
aortic  arches  appear,  in  the  second  and  third 
visceral  folds.  There  are  thus  in  the  chick 
five  pairs  of  aortic  arches,  corresponding  to 
the  anterior  five  of  the  six  pairs  found  in  the 
tadpole.  But  in  the  chick,  there  are  no  gill 
capillaries  at  any  stage  of  development ;  and 
there  is  never  any  distinction  between  the 
afferent  and  efferent  branchial  vessels,  the 
blood  flowing  through  one  continuous  vessel 
from  the  truncus  arteriosus  to  the  dorsal  aorta. 
The  condition  of  the  aortic  arches  in  the  chick 
embryo  is  more  comparable  to  the  condition 
in  the  frog  after  metamorphosis. 

The  main  changes  that  convert  the  arteries 
of  the  embryo  into  the  condition  which  they 
attain  in  the  adult  chick  are  the  following: 


244          Vertebrate  Embryology 

about  the  fourth  or  fifth  day,  the  middle 
parts  of  the  first  and  second,  the  mandibular 
and  hyoid,  aortic  arches  disappear.  The  lower 
ends  of  these  two  arches  persist  as  the  small 
mandibular  or  lingual  arteries  (Fig.  76,  A  L): 
while  their  upper  or  dorsal  ends  persist  as  the 
carotid  arteries,  each  of  which  immediately 
divides  into  an  internal  and  an  external 
branch  (Fig.  76,  A  C),  the  former  going  to 
the  brain  and  the  latter  to  the  face. 

By  the  sixth  day,  the  ventricular  septum  is 
complete,  and  its  front  edge  fuses  with  the 
hinder  edge  of  the  septum  that  divides  the 
truncus  arteriosus  into  right  and  left  sides. 
The  front  edge  of  this  latter  septum  arises 
between  the  fourth  and  fifth  aortic  arches  in 
such  a  way  that  all  of  the  blood  that  comes 
from  the  left  side  of  the  truncus  arteriosus 
(and  consequently  from  the  left  ventricle) 
passes  into  the  third  and  fourth  aortic  arches  ; 
while  the  blood  from  the  right  ventricle  passes 
into  the  fifth  aortic  arch. 

About  the  seventh  day,  the  right  and  left 
parts  of  the  truncus  arteriosus  separate  com- 
pletely from  each  other,  the  right  branch 
remaining  in  connection  with  the  fifth  aortic 
arch,  as  the  pulmonary  trunk ;  and  the  left 


Development  of  the  Fourth  Day    245 

branch  retaining  its  connection  with  the  third 
and  fourth  arches,  as  the  systemic  trunk. 

The  dorsal  communication  between  the  third 
and  forth  aortic  arches  (Fig.  76)  soon  becomes 
obliterated ;  and  the  ventral  ends  of  the  third 
arches  become  converted  into  the  subclavian 
arteries,  which  carry  blood  to  the  anterior 
appendages.  The  blood  from  the  left  side  of 
the  heart  now  passes  through  the  third  aortic 
arch  to  the  anterior  appendages,  and  through 
the  fourth  arch  to  the  dorsal  aorta.  The 
fourth  pair  of  aortic  arches  are  from  the  fifth 
day  much  larger  than  either  of  the  other  pairs 
that  are  still  present.  For  a  time  the  two 
arches  of  the  fourth  pair  are  of  the  same  size, 
but  the  arch  of  the  left  side  soon  begins  to 
diminish,  and  eventually  almost  completely  dis- 
appears ;  the  right  arch  increases  in  size  as 
the  left  diminishes,  and  forms  the  systemic 
arch  of  the  adult  chick.  It  is  to  be  noticed 
that  in  man  it  is  the  left  arch  that  persists  as 
the  systemic  arch. 

As  early  as  the  middle  of  the  third  day,  the 
pulmonary  arteries  are  formed  in  the  walls  of 
the  lungs,  and  when  the  fifth  pair  of  aortic 
arches  makes  its  appearance  the  pulmonary 
arteries  become  attached  to  and  open  into  the 


246          Vertebrate  Embryology 

ventral  ends  of  these  arches  (Fig.  76,  A  P). 
The  dorsal  end  of  the  fifth  arch  between  the 
point  of  union  of  the  pulmonary  artery  and 
the  dorsal  aorta  (Fig.  76,  A5)  is  known  as 
the  ductus  Botalli.  During  almost  the  entire 
period  of  incubation,  the  ductus  Botalli  re- 
mains open  and  offers  the  blood  from  the 
right  side  of  the  heart  an  easy  passage  into 
the  dorsal  aorta,  so  that  little,  if  any,  of  it 
passes  through  the  lung  capillaries.  At  the 
time  of  hatching,  the  ductus  Botalli  begins  to 
shrivel  up,  and  finally  becomes  entirely  closed, 
so  that  all  of  the  blood  from  the  right  side  of 
the  heart  must  pass  into  the  pulmonary  cir- 
culation. The  lower  half  of  the  fifth  aortic 
arch  then  becomes  the  pulmonary  artery. 

To  recapitulate  briefly.  The  dorsal  ends  of 
the  first  and  second  aortic  arches  persist  as  the 
carotid  arteries:  the  ventral  ends  of  these  two 
arches  persist  as  the  lingual  arteries.  The  ven- 
tral ends  of  the  third  arches  persist  as  the  sub- 
clavian  arteries.  The  fourth  arch,  on  the  right 
side,  persists  as  the  systemic  arch  ;  the  fourth 
arch,  on  the  left  side,  disappears.  The  ventral 
ends  of  the  fifth  arches  persist  as  the  pulmon- 
ary arteries. 

As  has  been  described,  the  two  dorsal  aortae, 


FlG.  76. — A  DIAGRAMMATIC  FIGURE  SHOWING  THE  ARRANGEMENT 
OF  THE  BLOOD  VESSELS  IN  A  CHICK  EMBRYO  AT  THE  END  OF  THE 
FIFTH  DAY  OF  INCUBATION.  THE  AMNION  HAS  BEEN  REMOVED,  AND 
THE  VITELLINE  VESSELS  CUT  SHORT  A  LITTLE  DISTANCE  FROM  THE 

EMBRYO.     (After  Marshall.) 

A,  dorsal  aorta.  A3,  A 4,  A 6,  third,  fourth,  and  fifth  aortic  arches  of  the 
right  side,  lying  in  the  first,  second,  and  third  branchial  arches  respectively.  A  A, 
allantoic  artery.  AB,  basilar  artery.  AC,  carotid  artery.  AH,  caudal  artery, 
the  terminal  portion  of  the  dorsal  aorta.  A  L,  lingual  artery.  AP,  pulmonary 
artery.  A  V,  vitelline  artery.  El,  auditory  vesicle.  RA ,  right  auricle.  RS, 
sinus  venosus.  R T,  truncus  arteriosus.  RV,  right  ventricle.  TA,  allantois. 
VA^  allantoic  vein.  VB,  anterior  cardinal  vein.  VC,  posterior  cardinal  vein. 
VD,  Cuvierian  vein.  VE,  meatus  venosus.  VH,  efferent  hepatic  vessel.  VI, 
posterior  vena  cava.  VJ,  jugular  vein.  VO,  afferent  hepatic  vessel.  VV^  vitel- 
line vein. 


247 


248          Vertebrate  Embryology 

formed  by  the  fusion  of  the  dorsal  ends  of  the 
aortic  arches  are  at  first  separate  from  each 
other  throughout  their  entire  length  ;  and  each 
gives  off  from  its  posterior  half  a  large  vitel- 
line  artery  which  carries  the  blood  to  the 
vascular  area  (Fig.  65,  Of. A).  By  the  end 
of  the  second  day  the  two  aortse  have  met  and 
fused  for  a  short  distance,  in  the  middle  region 
of  the  embryo  ;  and  by  the  fourth  day  this 
fusion  has  become  much  more  extensive,  and 
extends  backwards  beyond  the  point  where 
the  vitelline  arteries  are  given  off.  By  this 
time  the  roots  of  the  two  vitelline  arteries 
have  united,  for  a  short  distance,  into  a  com- 
mon trunk  (Fig.  76,  A  V}  ;  and,  of  the  two 
vitelline  arteries  into  which  this  common  trunk 
quickly  divides,  the  left  is  much  the  larger. 

Some  distance  posterior  to  the  point  of 
origin  of  the  vitelline  artery,  and  just  back  of 
the  point  of  separation  of  the  two  dorsal  aortae, 
the  allantoic  or  umbilical  arteries  arise  (Fig. 
76,  A  A).  Through  them  the  blood  passes  to 
the  allantois,  as  the  name  would  lead  one  to 
infer.  The  left  allantoic  artery  is,  from  the 
first,  generally  the  larger,  and  it  eventually 
carries  all  of  the  blood  to  the  allantois,  as  the 
right  artery  entirely  disappears. 


Development  of  the  Fourth  Day    249 

The  vitelline  and  allantoic  arteries  are,  of 
course,  purely  embryonic  structures,  and  dis- 
appear at  the  time  of  hatching,  when  the  yolk 
has  all  been  absorbed  or  taken  into  the  digest- 
ive tract,  and  the  allantois  is  cast  off  and  left 
in  the  shell. 

From  the  hinder  region  of  the  dorsal  aorta 
are  given  off  arteries  that  carry  the  blood  from 
the  left  side  of  the  heart  to  the  various  struct- 
ures of  the  abdominal  cavity. 

The  changes  that  take  place  in  the  venous 
system  are,  if  anything,  rather  more  compli- 
cated than  those  that  have  just  been  described 
in  connection  with  the  arteries  ;  but  if  each 
step  in  the  development  be  understood,  there 
should  be  no  difficulty  in  understanding  the 
entire  process  ;  and  a  clearer  understanding  of 
the  adult  circulation  can  be  obtained  by  the 
study  of  its  development  than,  perhaps,  in  any 
other  way. 

The  development  of  the  venous  system  has 
been  described  for  the  first  three  days  of  incu- 
bation. At  the  end  of  the  third  day,  it  will  be 
remembered,  the  blood  entered  the  auricular 
portion  of  the  heart  through  the  large  vein 
that  was  called,  in  its  entirety,  the  meatus 
venosus.  The  meatus  venosus  was  largely 


250          Vertebrate  Embryology 

formed  by  the  union  of  the  two  large  vitelline 
veins,  bringing  blood  back  from  the  vascular 
area,  but  also  received  blood  from  the  anterior 
end  of  the  body  of  the  embryo  through  the  two 
anterior  cardinal  veins,  and  from  the  posterior 
end  of  the  embryo  through  the  posterior  car- 
dinal veins.  The  anterior  and  posterior  cardi- 
nals of  each  side  unite  with  each  other,  just 
before  emptying  into  the  meatus  venosus,  to 
form  the  short  ductus  Cuvieri  (Fig.  66,  dc). 

The  anterior  and  posterior  cardinal  veins, 
during  the  earlier  stages  of  development,  bring 
back  the  blood  to  the  heart  from  practically 
all  parts  of  the  body  except  from  the  digestive 
organs. 

The  anterior  cardinals  persist  as  the  jugular 
veins,  being  joined,  at  an  early  period,  by  the 
pectoral  veins  from  the  anterior  appendages, 
and  the  vertebral  veins  from  the  head  and  neck. 

So  long  as  the  Wolffian  bodies  remain  func- 
tional, the  posterior  cardinals  retain  their  large 
size  ;  but  when  the  permanent  kidneys  become 
functional,  these  veins  diminish  in  size  and 
ultimately  disappear. 

The  ducti  Cuvieri  or  Cuvierian  veins  persist 
as  the  anterior  vence  cavcz  of  the  adult  chick 
(Fig.  78,  V.S.L.  and  V.  S.  R.). 


Development  of  the  Fourth  Day    251 

It  now  remains  to  describe  the  development 
of  the  system  of  the  posterior  (inferior)  vena 
cava,  which  is  an  evolution,  chiefly,  of  the 
meatus  venosus,  whose  formation  by  the  union 
of  the  two  vitelline  veins  has  already  been 
described  (Fig.  66). 

The  meatus  venosus,  from  its  first  forma- 
tion, is  closely  associated  with  the  liver.  The 
diverticula  from  the  digestive  tract  that  form 
the  liver  lie  close  to  the  meatus  venosus,  and 
as  they  grow  they  completely  surround  it. 
Soon  after  its  formation,  blood  vessels  begin  to 
develop  in  the  liver,  and  by  the  fifth  day  they 
have  opened  into  the  meatus  venosus  in  the 
following  manner  :  just  after  entering  the 
posterior  edge  of  the  liver,  the  meatus  veno- 
sus gives  off  a  collection  of  afferent  hepatic 
vessels,  through  which  some  of  the  blood, 
passing  towards  the  heart  from  the  vascular 
area,  may  enter  the  capillaries  that  are  formed 
in  the  substance  of  the  liver.  Just  before  leav- 
ing the  anterior  edge  of  the  liver,  the  meatus 
venosus  is  joined  by  a  collection  of  blood 
vessels,  the  efferent  hepatic  vessels  whose 
capillary  terminations  are  in  communication 
with  the  capillaries  of  the  afferent  hepatic 
vessels.  The  blood  that  passes  through  the 


252  Vertebrate  Embryology 

liver  has  now  two  courses  open  to  it ;  most  of 
it  passes  directly  through  the  large  meatus 
venosus  to  the  heart ;  but  a  part  passes,  by- 
way of  the  afferent  hepatic  vessels,  into  the 
substance  of  the  liver,  to  be  collected  and 


FIG.  77. — DIAGRAM  OF  THE  VENOUS  CIRCULA- 
TION AT  THE  COMMENCEMENT  OF  THE  FIFTH  DAY. 
(After  Foster  and  Balfour.) 

H,  heart,  d.c.,  ductus  Cuvieri  j  into  the  ductus  Cuvieri  of 
each  side  fall  /,  the  jugular  vein,  W,  the  wing  vein,  and 
c,  the  inferior  cardinal  vein.  S.V.,  sinus  venosus.  Of,  vitel- 
line  vein.  £7,  allantoic  vein,  which,  at  this  stage,  gives  off 
branches  to  the  body-walls.  F.C.7.,  inferior  vena  cava.  /, 
liver. 

brought  back  to  the  meatus  venosus  again  by 
the  efferent  hepatic  vessels  (Fig.  77). 

The  part  of  the  meatus  venosus  in  the  liver 
between  the  openings  of  the  afferent  and  effer- 
ent hepatic  vessels  is  generally  called  the 
ductus  venosus. 

By  the  fourth  day,  the  allantois  has  reached 
a  considerable  size,  and  in  it  are  developed 


Development  of  the  Fourth  Day    253 

the  two  allantoic  veins.  These  veins  unite  on 
entering  the  body,  to  form  a  single  vein  that 
empties  into  the  left  or  persistent  vitelline 
vein.  During  the  earlier  stages,  while  the 
yolk-sac  is  still  large,  and  the  allantois  is  small, 
the  allantoic  vein  is  much  smaller  than  the 
vitelline  vein,  and  seems  to  be  a  branch  of 
it,  (Fig.  76)  ;  but,  as  the  allantois  increases 
in  size  and  the  yolk-sac  diminishes,  the  rela- 
tive size  of  the  two  veins  becomes  reversed, 
and  the  vitelline  vein  seems  to  be  a  branch 
of  the  allantoic  (umbilical)  vein  (Fig  77). 
At  the  time  of  hatching,  of  course,  both 
veins  disappear.  During  the  fourth  day,  the 
veins  from  the  walls  of  the  hinder  part  of 
the  digestive  tract  unite  to  form  one  vein,  the 
mesenteric  vein.  This  vein  is  at  first  small  and 
empties  into  the  vitelline  vein  just  before  the 
latter  enters  the  liver  (Fig.  78,  M),  or  at  the 
point  where  it  may  be  said  to  become  the  mea- 
tus  venosus.  The  blood  that  enters  the  liver 
is,  therefore,  derived  from  three  sources:  (i) 
through  the  vitelline  vein,  from  the  yolk-sac  ; 
this  blood  is  rich  in  food  material,  and  has 
been  more  or  less  oxidized  in  the  vascular 
area ;  (2)  through  the  allantoic  vein,  from  the 
allantois  ;  this  blood  is  rich  in  oxygen  ;  (3) 


254          Vertebrate  Embryology 

through  the  mesenteric  vein,  from  the  diges- 
tive tract  of  the  embryo  ;  this  blood  is  venous 
in  character. 

As  the  embryo  increases  in  size,  the  mesen- 
teric vein  also  increases,  and  after  the  disap- 
pearance of  the  vitelline  and  allantoic  veins, 
at  .the  time  of  hatching,  it  persists  as  the 
hepatic  portal  vein  of  the  adult,  which  brings 
the  blood  from  the  hinder  parts  of  the  diges- 
tive canal  to  the  liver. 

The  posterior  (inferior)  vena  cava,  proper, 
arises  about  the  fourth  day,  between  the  hinder 
ends  of  the  Wolffian  bodies,  and  runs  forward 
in  the  middle  line,  ventral  to  the  dorsal  aorta. 
Anteriorly  it  joins  the  meatus  venosus  be- 
tween the  heart  and  the  anterior  edge  of  the 
liver  (Fig.  77,  V.  C.  /.)  ;  and  posteriorly,  it 
becomes  connected  with  the  permanent  kid- 
neys or  metanephra,  as  soon  as  the  latter  are 
formed,  and  with  the  hind  limbs  and  the  caudal 
region.  The  posterior  cava  is  at  first  a  small 
and  insignificant  vessel,  but  as  more  and  more 
blood  is  sent  to  the  heart  from  the  kidneys 
and  from  the  hinder  parts  of  the  body,  this  ves- 
sel becomes  larger  than  the  meatus  venosus, 
of  which  it  was  at  first  merely  a  branch. 

Before  this  change  in  the   relative   size   of 


Development  of  the  Fourth  Day    255 

the  two  vessels  has  been  entirely  accomplished, 
the  efferent  hepatic  vessels  shift  their  position 
so  as  to  open  directly  into  the  posterior  cava, 
instead  of  into  the  meatus  venosus  (Fig.  78)  ; 
and,  before  the  time  of  hatching,  the  part  of  the 
meatus  venosus  between  the  heart  and  the  liver 
becomes  obliterated,  so  that  all  of  the  blood 
that  flows  into  the  posterior  end  of  the  liver, 
through  the  portal  vein,  empties  into  the  pos- 
terior cava  through  the  hepatic  vein  (Fig.  79). 

One  thing  that  is  sometimes  confusing  in 
trying  to  trace  the  development  of  the  circu- 
latory system  by  studying  a  series  of  figures 
like  those  in  the  text,  is  the  variation  in  the 
relative  sizes  of  the  different  vessels ;  if  this 
feature  be  kept  in  mind,  it  may  help  to  make 
the  relationships  between  the  successive  stages 
more  evident. 

The  more  important  features  in  the  develop- 
ment of  the  blood  vessels,  from  their  earliest 
beginning  to  the  adult  condition,  have  now 
been  described  ;  and  it  may  help  to  make  the 
whole  subject  more  clear  if  a  brief  description 
be  given  of  the  course  of  the  circulation  during 
the  latter  part  of  the  period  of  incubation, 
together  with  the  changes  taking  place  at  the 
time  of  hatching. 


256          Vertebrate  Embryology 

The  course  of  the  circulation  at  the  end  of 
the  third  day  has  already  been  described 
(page  201),  and  need  not  be  repeated  at  this 
place,  so  that  we  shall,  at  once  proceed  to  the 


V.CJ 


FIG.  78. — DIAGRAM  OF  THE  VENOUS  CIRCULA- 
TION DURING  THE  LATER  DAYS  OF  INCUBATION. 
(After  Foster  and  Balfour.) 

H,  heart.  V.S.R,  right  vena  cava  superior.  V.S.L,  left 
vena  cava  superior.  The  two  venae  cavae  superiores  are  the 
original  "ducti  Cuvieri " ;  they  still  open  into  the  sinus 
venosus  and  not  independently  into  the  heart,  y,  jugular 
vein.  Su.V,  superior  vertebral  vein.  /#.  F,  inferior  vertebral 
vein.  W,  wing  vein.  F.C.7,  vena  cava  inferior,  which  re- 
ceives most  of  the  blood  from  the  inferior  extremities,  etc. 
D.V,  ductus  venosus.  /*.  F,  portal  vein.  M^  vein  from  intes- 
tines to  portal  vein.  Of,  vitelline  vein.  £/,  allantoic  vein  ; 
the  three  last-mentioned  veins  unite  to  form  the  portal  vein. 
/,  liver. 

description  of  the  circulation  as  it  is  during 
the  latter  part  of  the  period  of  incubation. 

"  The  heart  is  now  fully  formed.  The  sinus  venosus 
has  become  absorbed  into  the  right  auricle,  of  which  it 
now  forms  part:  the  auricular  septum  is  still  incomplete, 
the  large  foramen  ovale  allowing  blood  to  pass  freely 
from  the  right  auricle  to  the  left  auricle.  The  ventricular 


Development  of  the  Fourth  Day    257 

septum  is  complete;  and  the  truncus  arteriosus  is  di- 
vided into  two  entirely  separate  vessels,  of  which  one, 
the  pulmonary  trunk,  arises  from  the  right  ventricle,  and 
the  other  or  systemic  trunk  from  the  left  ventricle. 


SuV 


C.V 

FIG.  79.— DIAGRAM  OF  THE  VENOUS  CIRCULA- 
TION OF  THE  CHICK  AFTER  THE  COMMENCEMENT  OF 
RESPIRATION  BY  MEANS  OF  THE  LUNGS.  (After 

Foster  and  Balfour.) 

^  W^  wing  vein,  y,  jugular  vein.  Su.V^  superior  vertebral 
vein.  /«.£',  inferior  vertebral  vein.  These  unite  on  each 
side  to  form  the  corresponding  superior  vena  cava.  L  V^  pul- 
monary veins.  V.C.I,  vena  cava  inferior.  HP*  hepatic 
veins.  P.V,  portal  vein.  M,  mesenteric  veins.  Cy.M^ 
connecting  vessel  between  the  branches  of  the  portal  and  the 
system  of  the  vena  cava  inferior.  The  ductus  venosus  has 
become  obliterated.  The  three  venae  cavae  fall  independently 
into  the  right  auricle,  and  the  pulmonary  veins  into  the  left 
auricle.  CV,  crural  vein,  k*  kidney.  /,  liver,  pp^  hypo- 
gastric  veins.  C.V,  canal  vein.  V.S.L  and  V.S.R,  left  and 
right  venae  cavae  superiores. 

"  Three  pairs  of  aortic  arches  are  present,  but  these  are 
the  third,  fourth,  and  fifth  of  the  complete  series,  the 
first  and  second  having  disappeared  along  the  greater 
part  of  their  length.  The  systemic  trunk,  arising  from 

the  left  ventricle,  leads  to  the  third  and  fourth  pairs  of 
17 


258          Vertebrate  Embryology 

aortic  arches,  and  through  these  to  the  head  and  fore- 
limbs.  The  pulmonary  trunk,  arising  from  the  right 
ventricle,  leads  to  the  fifth  pair  of  aortic  arches,  which 
are  directly  continuous  with  the  dorsal  aorta  of  the  body 
of  the  embryo,  and  from  which  also  the  small  pulmonary 
arteries  arise.  From  the  aorta  a  vitelline  artery  carries 
blood  to  the  yolk-sac;  and  a  still  larger  allantoic  artery 
runs  from  the  aorta  to  the  allantois. 

"  The  blood  is  brought  back  to  the  heart  by  three 
veins:  —  the  right  and  left  anterior  venae  cavae,  and  the 
posterior  vena  cava.  The  right  and  left  anterior  venae 
cavae  return  blood  from  the  head  and  fore-limbs  of  the 
embryo.  The  posterior  vena  cava  returns  blood  from 
the  hinder  part  of  the  body,  the  limbs,  and  the  kidneys; 
just  before  reaching  the  heart  it  is  joined  by  the  ductus 
venosus,  which  returns  blood  from  the  yolk-sac,  from 
the  allantois,  and  from  the  alimentary  canal  of  the 
embryo,  by  the  vitelline,  allantoic,  and  mesenteric  veins, 
respectively.  The  blood  in  the  vitelline  vein  is  arterial 
as  regards  nutrient  matter;  the  blood  in  the  allantoic 
vein  is  arterial  as  regards  its  gaseous  components;  and 
the  blood  in  the  mesenteric  vein  is  venous.  The  blood 
in  the  posterior  vena  cava  is  venous  as  regards  nutri- 
ment, and  as  regards  gaseous  components,  but,  having 
just  passed  through  the  kidneys,  is  arterial  as  regards 
freedom  from  nitrogenous  excretory  matters. 

"The  blood  brought  to  the  heart  by  the  posterior 
vena  cava  may  therefore  be  spoken  of  as  arterial,  and 
stands  in  this  respect  in  marked  contrast  to  the  venous 
blood  brought  to  the  heart  by  the  right  and  left  anterior 
venae  cavse. 

"  All  three  vense  cavae  open  into  the  right  auricle  of 


Development  of  the  Fourth  Day    259 

the  heart:  but,  owing  to  the  position  and  direction  of 
the  opening,  and  to  the  Eustachian  valve,  the  arterial 
blood  from  the  posterior  vena  cava  is  directed  at  once 
through  the  foramen  ovale  into  the  left  auricle,  while 
the  venous  blood  from  the  right  and  left  anterior  venae 
cavae  remains  in  the  right  auricle.  The  right  auricle  is 
thus  filled  with  venous  blood,  and  the  left  auricle  with 
arterial  blood. 

"  On  contraction  of  the  auricles,  the  blood  they  contain 
is  driven  into  the  ventricles,  so  that  the  right  ventricle 
will  be  filled  with  venous,  and  the  left  with  arterial 
blood. 

"The  left  ventricle  drives  its  arterial  blood  along  the 
systemic  trunk,  and  through  the  third  and  fourth  pairs 
of  aortic  arches  to  the  head  and  fore-limbs;  while  the 
right  ventricle  forces  its  venous  blood  through  the  pul- 
monary trunk  and  fifth  pair  of  arches  into  the  dorsal 
aorta,  from  which  part  goes  to  supply  the  body  and  hind 
limbs  of  the  embryo,  and  part,  in  the  earlier  stages  by 
far  the  larger  part,  passes  out  along  the  vitelline  and 
allantoic  arteries  to  the  yolk-sac  and  allantois,  where  it 
takes  up  nutriment  and  oxygen. 

"  The  enormously  disproportionate  size  of  the  head  and 
anterior  part  of  the  embryo  and  the  stunted  condition 
of  the  hinder  part  during  the  earlier  stages  are  to  be 
ascribed,  at  any  rate  in  part,  to  this  arterial  supply  of 
the  anterior  half  as  contrasted  with  the  venous  supply  of 
the  posterior  half  of  the  embryo."  1 

The  changes  in  actual  structure  that  take 
place  at  the  time  of  hatching  are  comparatively 

1  Marshall. 


260          Vertebrate  Embryology 

slight,  but  they  produce  remarkable  changes  in 
the  course  of  the  circulation,  and  convert  the 
embryonic  circulation  just  described  into  that 
of  the  adult  chick. 

The  ductus  Botalli  or  ductus  arteriosus,  it 
will  be  remembered,  is  the  part  of  the  fifth 
aortic  arch  between  the  dorsal  aorta  and  the 
point  of  origin  of  the  vessel  that  runs  to  the 
lung  (Fig.  76,  A^).  So  long  as  this  vessel  re- 
mains open,  the  blood  from  the  right  ventri- 
cle can  pass  into  the  dorsal  aorta  and  thence 
to  the  hinder  part  of  the  body.  At  the  time 
of  hatching,  the  ductus  Botalli,  on  each  side 
of  the  body,  closes  up  entirely,  so  that  the 
blood  from  the  right  ventricle  must  now  pass 
through  the  pulmonary  arteries  to  the  lungs, 
and  thence,  by  the  pulmonary  veins,  back  to 
the  left  auricle. 

The  pulmonary  circulation  is  now  estab- 
lished ;  and  the  allantoic  circulation,  being  no 
longer  necessary  nor  possible,  ceases,  and  the 
allantoic  veins  and  arteries  disappear.  The 
yolk  being  entirely  absorbed  or  withdrawn  into 
the  now  completed  digestive  tract  there  is  no 
further  use  for  the  vitelline  veins  and  arteries, 
and  they  also  disappear.  By  the  disappear- 
ance of  the  allantoic  and  vitelline  vessels,  the 


Development  of  the  Fourth  Day    261 

entire  supply  of  blood  to  the  liver  is  derived 
from  the  mesenteric  vein,  by  which  it  is  brought 
from  the  hinder  part  of  the  digestive  tract ;  the 
mesenteric  vein  may  now  be  called  the  hepatic 
portal  vein. 

The  closure  of  the  ductus  venosus,  by  which 
all  of  the  blood  brought  to  the  liver  by  the 
portal  vein  is  compelled  to  pass  through  the 
hepatic  capillaries  before  reaching  the  heart, 
has  already  been  mentioned. 

It  is  not  until  some  time  after  hatching  that 
the  complete  closure  of  the  foramen  ovale  (the 
opening  between  the  right  and  left  auricles) 
takes  place.  By  the  closure  of  this  opening, 
all  of  the  blood  brought  to  the  heart  by  all 
three  venae  cavae  is  emptied  into  the  right 
auricle ;  and  when  that  auricle  contracts,  all  of 
this  blood  is  forced  into  the  right  ventricle, 
none  of  it  finding  its  way  directly  into  the  left 
auricle.  As  a  result  of  this,  also,  all  of  the 
blood  that  gets  into  the  left  auricle,  and,  con- 
sequently, into  the  left  ventricle,  comes  from 
the  lungs  by  the  pulmonary  veins.  Thus  are 
the  arterial  and  venous  streams  of  blood  com- 
pletely separated,  and  the  double  circulation 
is  established. 

Before  passing  to  the  development  of  the 


262          Vertebrate  Embryology 

fifth  day,  let  us  briefly  summarize  the  more 
important  events  of  the  fourth  day.  They 
are  : 

1.  Increase  in  the  body  and  cranial  flexure. 

2.  Growth  of  the  allantois. 

3.  Growth  of  the  tail-fold. 

4.  Appearance  of  the  limbs  as  local  thicken- 
ings of  the  Wolffian  ridge,  just  back  of  the 
heart  and  just  in  front  of  the  tail. 

5.  Opening  of  the   mouth,  by  the  absorp- 
tion of  the  partition  between  the  stomodaeum 
and  the  pharynx. 

6.  Development  of  the  olfactory  grooves. 

7.  Vacuolation  of  the  cells  of  the  notochord. 

8.  Beginning  of  the  vertebral  column. 

9.  Development  of  the  ureter. 

10.  Development  of  the  duct  of  Miiller. 

11.  Development    of    the    primitive   germ 
cells  in  the  genital  ridge. 

1 2.  Appearance  of  a  fourth  and  a  fifth  pair 
of  aortic  arches,  and  the  partial  disappearance 
of  the  first  and  second  arches. 

13.  Growth  of  the  septa  dividing  the  heart 
into  right  and  left  sides. 


CHAPTER    VII 

THE    DEVELOPMENT    OF   THE    FIFTH    DAY 

THERE  are  no  very  striking  features  to 
be    noticed   during    the   fifth   day,  the 
changes  that  take  place  being  mostly 
the  growth  and  development  of  the  structures 
that  have  originated  during  the  previous  days. 

The  allantois  is  now  a  large  and  vascular 
sac,  stretching  over  the  right  side  of  the  chick, 
between  the  two  layers  of  the  amnion  (Figs. 
38,  and  80,  all),  and  serving  as  the  chief  organ 
of  respiration. 

The  yolk  is  completely  enclosed  by  the 
blastoderm,  and  the  vascular  area  covers  about 
two-thirds  of  the  blastoderm.  The  embryo  is 
so  much  curved  that  its  head  and  tail  are 
almost  in  contact  (Fig.  80). 

The  splanchnic  stalk  is  completely  closed, 
and  will  remain  in  about  the  same  condition 
until  nearly  the  time  of  hatching  :  there  is  still 
considerable  space  between  it  and  and  the 
somatic  stalk. 

263 


264          Vertebrate  Embryology 

The  limbs. — During  this  day  the  limbs  in- 
crease considerably  in  size,  and  become  marked 
off  into  two  parts:  a  more  rounded  proximal 
portion,  and  a  somewhat  expanded  extremity. 
In  the  expanded  extremity  the  digits  are  be- 
ginning to  be  outlined  in  cartilage,  and  the 
rounded  proximal  portions  are  slightly  bent  to 
form  the  first  indications  of  the  elbow-  and 
knee-joints. 

The  angles  of  the  elbow  and  knee  are  at 
first  directed  almost  straight  out  from  the 
body,  but  at  about  the  eighth  day  both  limbs 
rotate,  so  that  the  elbow-joint  now  points 
backwards,  while  the  knee-joint  is  directed 
forwards  (Fig.  72,  B\  As  the  result  of  this 
rotation,  the  digits  of  the  anterior  appendage 
are  pointed  directly  forwards,  while  those  of 
the  leg  are  directed  backwards.  About  the 
tenth  day,  however,  the  hand  and  foot  ro- 
tate on  the  arm  and  leg,  so  that  the  digits  of 
the  former  are  directed  backwards,  and  the 
digits  of  the  latter  forwards.  By  the  end  of 
the  tenth  day,  the  appendages  have  the  out- 
lines of  well-developed  wings  and  legs,  except 
for  the  absence,  as  yet,  of  the  feathers  and  nails. 

The  bony  skeleton  is  early  outlined  in  car- 
tilage, which  later  becomes  ossified.  In  the 


Development  of  the  Fifth  Day    265 

manus  are  three  well-formed  digits,  with  a 
possible  fourth,  in  a  very  rudimentary  condi- 
tion. The  pes  has  three  well-formed  digits, 
and  two  others  that  are  in  a  more  or  less 
rudimentary  condition. 

The  ribs  and  sternum. — The  ribs  originate 
as  cartilaginous  bars  in  the  mesoblast  of  the 
body-wall.  By  the  fusion  of  the  ventral  ends 
of  certain  of  these  ribs,  two  longitudinal  carti- 
laginous bars  are  formed,  lying  side  by  side  in 
the  ventral  body-wall.  These  bars  later  seg- 
ment off  from  the  ribs  from  which  they  were 
formed,  and  by  fusing  with  each  other  form  a 
median  band  of  cartilage,  the  sternum. 

The  skull. — It  probably  will  not  be  practica- 
ble for  the  beginner  in  vertebrate  embryology 
to  work  out,  in  the  laboratory,  the  details  of  the 
development  of  the  skull ;  but  the  main  fea- 
tures will  be  given  at  this  time,  since  it  is  at 
(Fig.  72)  about  this  period  that  the  changes  to 
be  discussed  begin  to  take  place. 

It  is  convenient  to  discuss  the  development 
of  the  skull  under  two  heads  :  (i)  the  cranium 
proper ;  (2)  the  skeleton  of  the  visceral  arches. 

The  cranium  proper.  —  The  notochord, 
which,  as  has  been  said,  formed  a  sort  of  nu- 
cleus around  which  the  centra  of  the  vertebral 


266          Vertebrate  Embryology 

column  were  formed,  forms  also  a  part  of  the 
cranium.  It  extends  in  the  middle  line  along 
the  under  (ventral)  side  of  the  brain  as  far 
forward  as  the  hinder  edge  of  the  pituitary 
body.  On  each  side  of  this  anterior  part 
of  the  notochord  is  developed  a  horizontal 


all 

FIG.  80. — EGG  OF  CHICK  WITH  EMBRYO  AND 
FCETAL  APPENDAGES.  (After  Parker  and  Haswell, 
from  Duval.) 

a,  air-space,  a//,  allantois.  am,  amnion.  ar.  vase,  area 
vasculosa.  emb^  embryo,  yk^  yolk-sac. 

sheet  of  cartilage.  These  two  sheets  of  car- 
tilage, the  parachordal plates,  lie  in  close  con- 
tact with  the  notochord,  and,  with  it,  form  a 
broad  floor  for  the  hind-  and  mid-brains.  The 
two  parachordal  plates  fuse  together,  above 
and  below  the  notochord,  thus  enclosing  the 
latter,  to  form  the  so-called  basilar  plate  which 
forms  the  floor  of  the  hinder  part  of  the  skull. 
To  the  sides  of  the  basilar  plate  are  fused  the 


Development  of  the  Fifth  Day    267 

auditory  capsules,  which  enclose  the  auditory 
organs.  The  floor  and  sides  of  the  hinder 
part  of  the  skull  are  formed  by  the  growth  of 
the  basilar  plate  and  the  auditory  capsules. 

The  floor  of  the  anterior  end  of  the  skull  is 
formed  chiefly  by  the  trabeculce  cranii.  These 
are  two  rather  short  and  slender  rods  that  lie 
in  front  of  the  notochord  and  are  continu- 
ous with  the  anterior  ends  of  the  parachordal 
plates.  They  lie  on  each  side  of  the  pituitary 
body,  and  fuse  together  in  front  of  it,  forming 
the  ethmoidal plate.  The  ethmoidal  plate  ex- 
tends forwards  to  the  tip  of  the  beak,  and  is 
fused,  anteriorly,  with  the  olfactory  capsules. 
The  interorbital  septum  develops  as  a  large 
vertical  plate  from  the  dorsal  surface  of  the 
ethmoidal  plate,  along  its  whole  median  line. 

The  above-described  structures  form  the 
cartilaginous  skull,  and,  as  incubation  proceeds, 
this  cartilage  is  gradually  changed  to  bone, 
and  forms  the  bones  of  the  floor  and  sides  of 
the  adult  skull.  These  bones  which  are  first  out- 
lined in  cartilage  are  known  as  cartilage  bones. 

The  roof  of  the  skull,  the  parietals,  frontals, 
etc.,  is  chiefly  made  up  of  the  so-called  mem- 
brane bones,  that  is,  of  bones  that  are  not  pre- 
formed in  cartilage. 


268          Vertebrate  Embryology 

The  skeleton  of  the  visceral  arches. — The  de- 
velopment of  this  part  of  the  skeleton  is  also 
very  difficult  to  follow,  and  need  only  be  men- 
tioned, at  this  point,  as  it  has  already  been  dis- 
cussed in  connection  with  the  fate  of  the  visceral 
clefts  and  folds.  It  will  be  remembered  that 
it  was  the  jaws  and  the  hyoid  apparatus  that 


FIG.  81. — Two  VIEWS  OF  THE  HEART  OF  A  CHICK  ON  THE  FIFTH 
DAY  OF  INCUBATION.  (After  Foster  and  Balfour.) 

A,  from  the  ventral,  B,  from  the  dorsal  side.  /.#,  left  auricular  appendage. 
r.a,  right  auricular  appendage,  r.v^  right  ventricle.  /.z>,  left  ventricle.  £,  bul- 
bus  arteriosus. 

were  especially  concerned  in  the  development 
of  the  visceral  skeleton.  It  is  the  enormous 
forward-growth  of  the  jaws  that  is  largely  re- 
sponsible for  the  characteristic  outline  to  the 
face  of  the  chick. 

The  heart. — The  fifth  day  is  one  of  the 
most  important  in  the  history  of  the  devel- 
opment of  the  heart.  The  most  important 


Development  of  the  Fifth  Day    269 

changes  in  the  heart  from  this  time  until  the 
time  of  hatching  will  now  be  mentioned. 

During  the  fifth  day  the  interventricular 
septum  is  completed,  and  becomes  fused  an- 
teriorly with  the  posterior  edge  of  the  septum 
that  is  developed  at  this  time,  in  the  truncus 
arteriosus.  This  latter  septum  is  attached, 


r. 


FIG.  82. — HEART  OF  A  CHICK  ON  THE  SIXTH  DAY 

OF  INCUBATION,  VENTRAL  SURFACE.       (After  Foster 

and  Balfour.) 


/.«,  left  auricular  appendage,    r.a,  right  auricular  append- 
ge.      r.v^  right  ventricle.      /.z>,  left  ventricle. 


anteriorly,  between  the  fourth  and  fifth  pairs 
of  aortic  arches,  and  follows  a  sort  of  spiral 
course  backwards,  to  where  it  joins  the  inter- 
ventricular  septum.  The  effect  of  these  septa 
in  directing  the  blood  from  the  right  and  left 
ventricles  into  different  channels  has  already 
been  explained  (page  244).  Before  the  com- 
pletion of  the  septum  of  the  truncus  arteriosus, 


270          Vertebrate  Embryology 

the  two  sets  of  semilunar  valves  have  been 
formed  between  the  two  divisions  of  the  trun- 
cus  and  the  two  ventricles  into  which  they 
open. 

During  the  next  two  or  three  days  the  heart 
continues  to  approach  more  nearly  the  shape 
of  the  adult,  though  there  is  no  remarkable 
change  in  structure. 

By  the  twelfth  day,  the  interauricular  sep- 
tum has  increased  to  such  an  extent  that  the 
opening  between  the  two  auricles  is  reduced 
to  a  small  opening,  the  foramen  ovale. 

Shortly  before  hatching,  the  foramen  ovale 
becomes  nearly  closed  by  a  membranous  fold  ; 
and  shortly  after  hatching,  the  closure  is  com- 
plete, and  the  heart  has  practically  the  adult 
structure. 

During  the  later  stages  of  incubation,  the 
walls  of  the  ventricles  and  auricles,  especially 
the  former,  become  much  thickened  by  the  in- 
ward growth  of  ridges  from  the  muscular  walls, 
forming  the  trabeculae  of  the  adult  heart.  The 
truncus  becomes  thickened  simply  by  the  in- 
crease in  the  thickness  of  the  component 
layers  of  its  walls. 

The  pericardial  and pleural  cavities. — It  will 
be  seen,  by  the  examination  of  figures  of  the 


msth. 


Ent. 


FIG.  83.— TRANSVERSE  SECTION  THROUGH  THE  DORSAL  REGION 
OF  A  CHICK  EMBRYO  WITH  ABOUT  TWENTY-EIGHT  SEGMENTS.  (After 
Minot.) 

Am.,  amnion.  A  a.,  aorta,  card.,  cardinal  vein.  Cho.,  chorion.  Coe.,  Coe' .,  coe- 
lom.  EC.)  ectoderm,  endo.,  endothelial  heart.  Ent.,  entoderm.  Z,/'.,  liver,  mes., 
mesoderm.  m.kt.,  muscular  heart,  msth.)  mesothelium.  My.,  primitive  seg- 
ment, nek.,  notochord.  raph.,  raphe  of  amnion.  Si.V.,  sinus  venosus  of  heart. 
Som.,  somatopleure.  Sp.c.,  spinal  cord.  Spl.,  splanchnopleure.  Ve.,  vein.  K, 
accumulation  of  mesodermic  material  about  the  vitelline  vein. 


27I 


272          Vertebrate  Embryology 

earlier  stages  in  the  development  of  the  chick, 
that  the  heart  at  first  has  no  special  cavity  of 
its  own,  but  lies  freely  in  the  general  body- 
cavity  (Figs.  55  and  57).  The  origin  of  the 
pericardial  cavity  is,  briefly,  as  follows  :  in  the 
plane  of  the  Cuvierian  veins,  where  they  cross 
the  body-cavity  from  the  somatopleure  to  the 
sinus  venosus,  is  developed  a  horizontal  mem- 
brane or  septum.  This  septum  evidently  di- 
vides the  body-cavity  into  an  upper  and  a 
lower  chamber,  in  the  latter  of  which  lies  the 
heart.  These  two  chambers  of  the  body- 
cavity  are  at  first  in  communication  with  each 
other  both  in  front  and  behind  the  horizontal 
septum  ;  but  the  anterior  edge  of  the  septum 
now  grows  forwards  and  upwards  until  it 
meets  and  fuses  with  the  ventral  wall  of  the 
fore-gut,  and  the  posterior  edge  grows  back- 
wards and  downwards  until  it  meets  the  ven- 
tral wall  of  the  body-cavity ;  the  space  in 
which  the  heart  lies  is  thus  separated  from  the 
rest  of  the  body-cavity,  and  becomes  the  per- 
icardial cavity. 

As  the  lungs  are  formed,  as  outgrowths 
from  the  anterior  part  of  the  digestive  tract, 
they  lie  in  the  dorsal  part  of  the  body-cavity, 
above  the  horizontal  septum,  and  on  each  side 


Development  of  the  Fifth  Day    273 

of  the  fore-gut.  As  they  continually  increase 
in  size,  they  gradually  force  the  horizontal  sep- 
tum down  on  each  side  of  the  heart,  until 
the  pericardial  cavity  is  reduced  to  very  nar- 
row limits  (Fig.  84,  p  c). 

These  spaces  in  which  the  lungs  lie  are  the 
pleural  cavities,  and  in  the  bird  they  remain 
continuous,  at  their  posterior  ends,  with  the 
general  body-cavity. 

Histological differentiation. — It  is  at  this  time 
that  histological  differentiation  may  be  said  to 
commence,  though  from  the  earliest  hours  of 
embryonic  life  the  cells  of  the  different  germ- 
layers  were  more  or  less  dissimilar. 

It  may  be  defined  as 

"  a  process  by  which  the  structure  of  the  cells  is  mod- 
ified, so  that  cells  become  dissimilar  in  structure  by 
acquiring  an  organization  which  adapts  them  to  spe- 
cial functions.  The  cells  which  arise  during  the  seg- 
mentation of  the  ovum  differ  but  slightly  from  one 
another.  As  development  progresses  we  find  the  cells 
change,  some  in  one  way,  some  in  another,  so  that 
many  kinds  of  cells  are  produced,  but  of  each  kind  we 
find  a  large  number  of  cells.  Each  kind  of  cell  may  be 
said,  roughly  speaking,  to  form  a  tissue  for  itself.  Cells 
of  each  tissue  offer  visible  peculiarities  by  which  they 
may  be  readily  distinguished  from  one  another  under  the 
microscope.  It  thus  appears  that  the  production  of 
tissues  is  the  main  result  of  differentiation,  so  that  this 


274          Vertebrate  Embryology 

process  of  development  may  be  fairly  accurately  de- 
fined as  equivalent  to  histogenesis.  As  to  the  factors 
which  cause  differentiation,  we  have  no  satisfactory 
knowledge.  We  can,  at  present,  only  note  the  changes, 


FIG.  84. — SECTION  THROUGH  AN  ADVANCED  EMBRYO  OF  A  RABBIT, 
TO  SHOW  HOW  THE  PERICARDIAL  CAVITY  BECOMES  SURROUNDED  BY 
THE  PLEURAL  CAVITIES.  (After  Foster  and  Balfour.) 

ht,  heart,  pc,  pericardial  cavity.  //./,  pleural  cavity.  Ig,  lung.  <?/,  alimentary 
tract.  a0,  dorsal  aorta,  ch^  notochord.  rp^  rib.  st,  sternum,  j/.r,  spinal  cord. 

when  they  acquire  such  magnitude  as  to  become  micro- 
scopically visible.  As  to  the  physiological  conditions 
which  cause  these  changes  we  have  almost  no  concep- 
tions. It  is  probable  that  the  nucleus  has  a  leading  role 
to  play,  but  our  knowledge  of  this  role  is  too  litte  ad- 
vanced to  permita  profitable  discussion  of  the  subject  here. 


Development  of  the  Fifth.  Day     275 

"  The  actual  process  of  differentiation  shows  itself 
both  in  the  protoplasm  and  in  the  nucleus  of  the  cell. 
The  changes  in  the  former  are  the  more  conspicuous, 
and  therefore  the  better  known.  The  changes  in  the 
nucleus  have  still  to  be  adequately  studied."  1 

According  to  Minot  there  are  two  types  of 
differentiation,  both  starting  from  the  same 
point  —  the  undifferentiated  embryonic  cell. 
In  the  first  type,  as  the  cells  are  proliferated 
certain  ones  are  differentiated  into  new  forms, 
while  the  rest  of  them  remain  undifferentiated 
and  retain  the  power  of  proliferation.  The 
epidermis  is  an  illustration  of  this  type.  Some 
of  the  cells  which  are  formed  by  the  multipli- 
cation of  its  lower  layer  pass  towards  the  sur- 
face and  differentiate  into  horny  cells ;  while 
other  cells  remain  at  the  base  of  the  epidermis 
and  continue  to  multiply.  In  the  second  type 
of  differentiation,  all  the  cells  become  at  once 
differentiated,  and  lose  partly  or  completely 
their  power  of  multiplication.  This  type  is 
illustrated  by  the  central  nervous  system.  The 
growth  of  the  brain,  after  the  earlier  stages, 
takes  place  by  the  growth  of  the  individual 
cells,  rather  than  by  the  increase  in  the  num- 
ber of  the  cells.  After  their  formation,  the 

1  Minot. 


276          Vertebrate  Embryology 

glia  cells  divide  but  slowly,  and  the  neurones 
not  at  all. 

It  should  be  noted  that,  according  to  the 
so-called  law  of  genetic  restriction,  "  differen- 
tiation acts  as  a  progressive  restriction  upon 
further  development.  Each  successive  stage 
of  differentiation  puts  a  narrower  limitation  up- 
on the  possibility  of  further  advance." 1  This 
may  be  illustrated  by  the  ectoderm.  This 
layer  early  shows  a  division  into  two  secondary 
layers,  the  epidermal  and  the  nervous.  The 
epidermal  layer  never  forms  nervous  structures, 
and  the  nervous  layer  never  forms  epidermal 
structures.  In  the  nervous  layer  are  soon  de- 
veloped nerve-cells  and  neuroglia  cells  ;  the 
former  never  develop  into  the  latter,  nor  the 
latter  into  the  former.  Similar  illustrations 
might  be  given  from  the  entodermal  and  me- 
sodermal  layers. 

One  of  the  first  changes  noticed  in  the 
ectoblast,  besides  the  separation  into  two  lay- 
ers, is  the  formation  of  certain  thickened  areas 
which  have  been  called  plakodes.  Examples 
of  these  local  thickenings  are  seen  in  the  eye, 
nose,  and  ear  invaginations  that  have  already 
been  described.  From  the  ectoderm  are  de- 

1  Minot, 


Development  of  the  Fifth  Day    277 

rived  the  following  organs — the  epidermis  and 
its  appendages  ;  the  lens  of  the  eye  ;  the  epi- 
thelium of  the  cornea ;  the  olfactory  chamber ; 
the  auditory  organ  ;  the  mouth,  and  the  anus  ; 
the  brain  ;  the  spinal  chord  ;  the  retina  ;  the 
optic  nerve  ;  the  nerve-fibres,  etc. 

The  entoderm  almost  from  the  first  exhibits 
two  or  three  kinds  of  cells,  found  in  the  area 
opaca,  area  pellucida,  and  embryo  proper. 
This  layer  also  shows  variations  in  thickness, 
analogous  to  those  seen  in  the  ectoderm. 
From  the  entoderm  are  developed  the  noto- 
chord,  and  the  epithelium  of  the  entire  res- 
piratory and  digestive  tracts  with  their 
appendages ;  the  epithelium  of  the  mouth  and 
anus,  however,  are  of  ectoblastic  origin,  as  has 
been  stated. 

The  mesoderm  early  shows  a  differentiation 
into  several  varieties,  which,  however,  are 
largely  due  to  the  method  of  grouping  or  the 
varying  degrees  of  condensation  of  the  cells. 
From  the  mesoderm  are  derived  all  the  struc- 
tures not  mentioned  in  connection  with  the 
other  two  germ-layers,  such  as  muscle,  bone, 
blood,  urogenital  organs,  etc. 

The  most  important  changes  in  the  develop- 
ment of  the  fifth  day  are  : 


278          Vertebrate  Embryology 

1.  Growth  of  the  allantois. 

2.  Growth  of  the  limbs,  and  the  appearance 
in  them  of  the  cartilages  and  of  the  elbow-and 
knee-joints. 

3.  Appearance  of  the  cartilaginous  cranium, 
and  of  the  bars  of  cartilage   in  the   visceral 
arches. 

4.  Development  of  parts  of  the  face. 

5.  Completion  of  the    ventricular   septum  ; 
and  the  appearance  of  the  septum  of  the  bul- 
bus  arteriosus,  and  of  the  semilunar  valves. 

6.  The  establishment  of  the  different  tissues. 


CHAPTER  VIII 

THE  DEVELOPMENT  FROM  THE  SIXTH  DAY 
TO  THE  TIME  OF  HATCHING 

The  sixth  and  seventh  days. — It  is  during 
this  period  that  the  distinctively  avian  charac- 
teristics make  their  appearance. 

Up  to  this  time  there  is  nothing  about 
the  embryo  that  would  enable  the  inexperi- 
enced eye  to  distinguish  the  chick  embryo 
from  that  of  many  other  and  quite  different 
animals  ;  and,  in  fact,  it  would  be  difficult,  if 
not  impossible,  for  even  an  experienced  eye 
to  distinguish  the  chick  embryo,  during  the 
very  early  stages,  from  other  embryos  at  a 
corresponding  state  of  development. 

It  is  at  this  time  that  the  nasal  region  be- 
gins to  lengthen,  and  the  anterior  and  pos- 
terior limbs  begin  to  take  on  the  form  of 
wings  and  legs  (Fig.  72,  B). 

The  amnion  does  not  now  lie  so  close  to 
the  embryo  as  during  the  earlier  stages,  and 
in  the  enlarged  amniotic  cavity  has  collected 

279 


280          Vertebrate  Embryology 

a  considerable  amount  of  fluid.  Slow,  rhythmic 
pulsations  are  seen  passing  over  the  amnion, 
caused,  probably,  by  the  contraction  of  the 
muscle-fibres  that  are  developed  in  the  meso- 
blastic  portion  of  the  amniotic  folds.  This 
pulsation  of  the  amnion  gives  to  the  embryo  a 
sort  of  rocking  motion  in  the  amniotic  fluid. 
At  a  later  period,  such  movements,  it  is  said, 
may  be  seen  in  the  allantois. 

The  allantois  has  increased  rapidly  in  size, 
and  contains  a  quantity  of  fluid.  Both  the 
vitelline  veins  and  arteries  now  pass  from  the 
body  as  single  vessels  ;  and  the  yolk,  though 
apparently  undiminished  in  quantity,  is  much 
more  fluid  than  during  the  earlier  days.  The 
flexure  of  the  body  is  less  marked  than  on 
previous  days ;  and  the  neck  is  becoming 
more  apparent.  The  disproportion  between 
the  size  of  the  head  and  that  of  the  rest  of  the 
body  is  being  reduced  by  the  more  rapid 
growth  of  the  body.  The  width  of  the  so- 
matic stalk  is  being  reduced,  with  the  result 
that  the  heart  is  being  enclosed,  and  no  longer 
seems  to  hang  loosely  out  of  the  body  :  in  the 
wall  of  the  body  thus  formed,  the  cartilaginous 
ribs  and  sternum  are  being  developed.  The 
growth  of  the  cerebral  hemispheres  has  been 


From  Sixth  Day  to  Hatching     281 

very  marked.  The  structures  around  the 
mouth  have  assumed  more  avian  outlines ; 
while  in  the  floor  of  the  mouth  the  tongue 
has  begun  to  develop,  as  a  bud  of  mesoblast 
covered  with  ectoblast. 

The  eighth,  ninth,  and  tenth  days. — About 
the  only  change  noticed  in  the  amnion  is  a 
diminution  in  the  intensity  of  the  pulsations, 
which  were  at  their  height  on  the  eighth  day, 
and  now  gradually  grow  less.  The  allantois 
covers  a  large  part  of  the  yolk-sac,  and  is  ex- 
tremely vascular,  especially  its  upper  layer 
which  lies  close  under  the  shell  membranes. 
The  yolk  is  beginning  to  diminish  rapidly, 
and  the  yolk-sac  is  becoming  wrinkled  and 
flabby.  The  little  sacs  containing  the  feathers 
begin  to  protrude  from  the  surface,  especially 
along  the  back,  of  the  rapidly  growing  embryo. 
On  the  tip  of  the  nose  is  seen  a  chalky  patch, 
the  beginning  of  the  horny  beak. 

The  eleventh  day  to  the  time  of  hatching. 
—By  the  eleventh  day,  the  abdominal  walls, 
though  much  less  firm  than  those  of  the  chest, 
may  be  said  to  be  fully  formed,  and  the  loops 
of  the  intestines  which  have  been  hanging 
down  loosely  are  enclosed  in  the  body-cavity. 
The  body  is  thus  completed  except  for  the 


282          Vertebrate  Embryology 

narrow  stalks  of  the  umbilicus  and  the  yolk- 
sac.  The  allantois  continues  to  increase  in 
prominence,  while  the  amnion  becomes  less 
conspicuous  on  account  of  the  disappearance 
of  the  amniotic  fluid. 

By  the  thirteenth  day,  the  feathers  are 
generally  distributed  over  the  body,  and  their 
form  and  color  may  be  seen  through  the  thin 
walls  of  the  sacs  in  which  they  are  still  en- 
closed. They  remain  enclosed  in  the  sacs 
until  the  nineteenth  day,  when  they  are  an 
inch  or  more  in  length. 

On  the  thirteenth  day,  nails  and  scales  ap- 
pear on  the  toes  ;  and  by  the  sixteenth  day, 
the  nails,  scales,  and  beak  are  all  quite  firm 
and  horny. 

By  the  thirteenth  day  the  cartilaginous 
skeleton  is  complete,  and  numerous  centres  of 
ossification  have  made  their  appearance. 

By  the  sixteenth  day,  the  white  of  the  egg 
has  disappeared,  and  the  cleavage  of  the  meso- 
blast  has  extended  entirely  around  the  yolk. 
On  the  nineteenth  day,  the  remains  of  the  yolk 
are  withdrawn  bodily  into  the  body-cavity, 
which  was  not  nearly  filled  by  the  loops  of  the 
intestine. 

The  changes  that  take  place  in  the  circulation 


From  Sixth  Day  to  Hatching      283 

during  the  latter  days  of  incubation  have  al- 
ready been  described,  and  need  not  be  men- 
tioned at  this  place. 

As  early  as  the  sixth  day,  movements  of  the 
chick  may  sometimes  be  noticed,  on  opening 
the  egg,  but  whether  they  are  purely  volun- 
tary, or  caused  by  the  effects  of  the  air  on  the 
opened  egg,  it  is  difficult  to  say.  Soon  after 
this  time  undoubted  voluntary  motions  do 
occur :  and  on  the  fourteenth  day,  the  embryo 
shifts  its  position,  so  that,  instead  of  lying 
transversely  to  the  long  axis  of  the  egg,  it 
comes  to  lie  with  its  head  towards  the  large 
end  of  the  egg,  which  brings  its  beak  close 
to  the  now  much-enlarged  air-space  that  was 
mentioned  in  the  description  of  the  unincu- 
bated  egg  (Fig.  33,  a  ).  About  the  twentieth 
day,  the  beak  is  thrust  into  the  air-space,  and 
the  chick,  for  the  first  time,  begins  to  breathe 
by  means  of  its  lungs.  As  the  pulmonary 
circulation  begins,  the  blood  ceases  to  flow 
into  the  umbilical  vessels,  and  the  allantois,  in 
consequence,  shrivels  up,  and  is  left  inside  the 
shell  as  the  chick  pecks  its  way  out  of  the  egg. 


INDEX 


Air  sacs  :  Chick,  209 
Air  space  :  Chick,  90 
Albumen  of  egg  :  Chick,  90. 
Alimentary  canal :  Frog,  45-51  ; 

Chick,  203-212 
Allantois  :  Chick,  161,  263 
complete   history    of :  Chick, 

169-172 
Amnion:  Chick,  117,    132,  160- 

161 
entire  history  of:  Chick,  167- 

169 

Amniotic  cavity:  Chick,  168 
Angioblast:   147 

Anterior  chamber :    Chick,    183 
Aortic  arches  :  Frog,  62  ;  Chick, 
145,     243  ;    (see     Branchial 
blood      vessels) 
fate  of  :  Chick,  246 
Archenteron  :  Frog,  25 
Archinephric  duct  ;  Frog,  78 
Area  opaca  :  Chick  104 
Area  pellucida  :  Chick,  104 
Artery,  allantoic  :  Chick  248 
carotid  :  Frog,  61  ;  Chick,  244 
lingual  :  Chick,  244 
mandibular  :  Chick,  244 
pulmonary  :  Chick,  245 
subclavian  :  Chick,  245 
umbilical  :    Chick  (see  Allan- 
toic artery) 

vitelline  :  Chick,  145,  248 
Auditory   capsules :    Frog,    77  ; 

Chick,  267 

Auditory  pits  :  Chick,  141 
Auditory     vesicle  :     Frog,     43 ; 
Chick,  185 


Auricle  :  Chick,  156 
Auricular  chamber  :  Frog,  61 

Basilar  plate  :  Frog,  75  ;  Chick, 

226 

Beak  :  Chick,  281 
Bladder  :   Frog,  50 
Blastoderm  :  Chick,  91,  103,  163 

section  of  :  Chick,  121 
Blastomere  :  Frog,  18 
Blastopore  :  Frog,  22,  46 
Blastula:  100 
Blood  :  Chick,  146-151 
corpuscles  :  (see  Blood) 
islands  :  Chick,  147 
vessels  :  Frog,  56-69  ;    Chick, 

146-151 
Body-cavity  :  Frog,   30,    69-72  ; 

Chick,  132 
Brain  :  Frog,  36-40  ;  Chick,  154, 

172-173 
Branchial    arch  :     (see    Visceral 

clefts  and  folds) 
Branchial  blood  vessels  :    Frog, 

62 
Branchial     cleft  :    (see    Visceral 

clefts  and  folds) 
Branchial    folds  :      (see  Visceral 

clefts  and  folds) 
Bulbus   arteriosus  :  Chick,    145, 

156 

Carotid  arch  :  Frog,  67 
Carotid  gland  :  Frog,  68 
Cartilage  bones  :  Chick,  267 
Centra  :  Frog,  73 


285 


286 


Index 


Cerebellum  :  Frog,    37  ;    Chick, 

224 
Cerebral      hemispheres  :     Frog, 

38  ;  Chick,  154,  224 
Chalazge  .  Chick,  91 
Choroid  coat  :  Chick,  181 
Choroid   fissure   or   slit  :    Frog, 

42  ;  Chick,  179 
Chromosome  :  12 
Cicatricula  :  (see  Blastoderm) 
Circulation, changes  in,  at  meta- 
morphosis :  Frog,  63-69 
Circulation,  changes  in,  at  time 
of    hatching  :    Chick,    259- 
261 
at  end  of  second  day  :  Chick, 

157-159 

of  third  day  :  Chick,   201-203 
at   end   of  third  day  :  Chick, 

256-261 

Cleavage  of   the   egg  :  (see  Seg- 
mentation of  the  egg) 
Cleavage  plane  :  Frog,  17 
Cloaca  :  Frog,  45-48  ;  Chick,  206 
Ccelom  :  (see  Body-cavity) 
Concrescence  :  24-25 
Conjunctival  epithelium:  Chick, 

183 

Cornea  :  Chick,  183 
Corneal  corpuscles  :  Chick,   183 
Cranial  flexure  :  Frog  36  ;  Chick, 

155,  167,  223 

Cranial  nerves  :    Chick,  155,  226 
Cranium  :     Frog,      75  ;    Chick, 

265-267 
Crura  cerebri  :  Frog,  37 

Development,  rate  of  :  Frog,  I  ; 

Chick,  1 20 

Discoidal  cleavage  :  97 
Dorsal  aorta  :  Frog,  61  ;  Chick, 

145 

Ductus   artenosus :    (see   Ductus 

Botalli) 

Ductus  Botalli :  Chick,   246,  260 
Ductus  Cuvieri  :    (see  Cuvierian 

vein) 


Ductus  venosus  :  Chick,  199 

closure  of  :  Chick,  261 
Duodenum  :  Chick,  206 

Ear  :   Frog,  43  ;  Chick,  184-187 
Ectoderm    or   ectoblast  :     Frog, 

24  ;  Chick,  104 
organs  from:  Frog,  31;  Chick, 

276-277 
Egg  :    Frog,    6-10,    88  ;    Chick, 

90-93  ;  Starfish,  5-6 
passage      through       oviduct : 

Chick,  94-95 
Eighth    day,    development    of  : 

Chick,  281 

Eleventh  day  to  hatching,  devel- 
opment of  :  Chick,  281-283 
Embryo,  change  in  position  of  : 

Chick,  165-167,  283 
cloth   model   of:  Chick,  114- 

119 
curvature  of  body  of  :  Chick, 

167 
estimation  of  age  of  :  Chick: 

134-135 

movements  of  :  Chick,  283 
rocking  motion  of  :  Chick,  169 
Embryo-sac  :  Chick,  116,  165 
Embryonic   shield :    Chick,    122 
Entoderm   or   entoblast  :    Frog, 

26  ;  Chick,  121 
organs  from:  Frog,  31;  Chick, 

.  2.77 
Epididymis  :  Chick,  236 

Equal  segmentation  :  97 
Ethmoidal  plate  :  Chick,  267 
Eustachian     tube :     Frog,     53  ; 

Chick,  193 

Eustachian  valve  :  Chick,  259 
Exoccipital  :  Frog,  77 
External  auditory  meatus :  Chick, 

193 
External  nares  :  Frog,  45;  Chick, 

187 
Eye  :  Frog,  41-43  ;  Chick,  175- 

184 
Eyelids  :  Chick,  183 


Index 


287 


Fallopian  tube  :  (see  Oviduct) 
False  amnion  :  Chick,  168 
Fat  bodies  :   Frog,  88 
Feathers:  Chick,  281-282 
Female  pronucleus  :  Frog,  n 
Fertilization  of  the  egg  :   Frog, 

16-17  J  Chick,  95 
Fifth     day,     development     of : 

Chick,  263-278 
First     day,     development      of : 

Chick,  120-139 
Foramen  ovale  of  heart  :  Chick, 

256-261 
Fore-brain :    Frog,    37 ;    Chick, 

141 

Fore-gut :  Chick,  131,  203 
Fourth     day,   development    of : 

Chick,  222-262 
Fourth  ventricle  :  Frog,  37 
Frontal  bone  :  Frog,  77 
Fronto-nasal  process  :  Chick,  195 

Gastrula  :  100 

Gastrulae,  kinds  of  :   100-102 

Gastrulation,  relation  to  amount 

of  yolk  :  98-103 

Genetic  restriction,  law  of :  276 
Genital   organs  :    Frog,    87-89  ; 

Chick,  237-241 
Genital  ridge  :  Frog,  87  ;  Chick, 

237,  239 
Germ  layers,  fate  of :  Frog,  30— 

31  ;  Chick,  276-277 
formation    of:    Frog,     21-30 ; 

Chick,  103-104,  121-127 
Germinal  disc  :  Chick,  94 
Germinal     vesicle :     Frog,      7  ; 

Chick,  94  ;  Starfish,  6 
Gill   clefts   and    folds,    develop- 
ment and  fate  of  :  Frog,  51- 

56;  Chick,  192-198 
Gill  pouch  :  (see  Gill  clefts  and 

folds) 
Gills,    external     and     internal : 

Frog,   53-56 
Gizzard  :  Chick,  207 
Glomerulus  :  Frog,  82 


Glottis  :  Chick,  209 

Gonoblast :    Frog,    88 ;    Chick, 

239-240 
Graafian  follicle  :  Chick,  240 

Harelip  :   196 
Hatching  :  Chick,  283 
Head  :  Chick,  224-226 
Head-fold  :  Chick,  130-131,  160 
Head-kidney :       Frog,      78-82 ; 

Chick,  233-234 
fate  of:  Frog,  81-82;  Chick, 

236 

Heart  :    Frog,     56-69 ;     Chick, 
143, 155,  198, 241-242,  268- 
270 
beginning    of    pulsations    of: 

Chick,  145 

and     blood  vessels,     develop- 
ment of :   Frog,  56-69 
endothelial  lining  of  :  Frog,  58 
looping  of  :  Chick,  144 
musculature  of  :  Frog,  60 
Hind-brain  :    Frog,    37  ;   Chick, 

141 

Hind-gut :  Chick,  203 
llistological  differentiation:  273- 

277 

types  of  :  275 
Holoblastic  segmentation  :    (see 

Segmentation,  complete) 
Hyoid  apparatus  :  Chick,  194 
Hyoid  arch  :  Frog,  51  ;  Chick, 

191 
Hyomandibular  cleft:  Frog,  51  ; 

Chick,   191 

Infundibulum  :  Frog,  37 
Interauricular    septum :    Chick, 

270 
Intermediate   cell-mass:    Chick, 

216 

Interorbital  septum  :  Chick,  267 
Interventricular  septum  :  Chick, 

269 
Invagination  :  Frog,  22  ;  Chick, 

130-131 
Iris  :  Chick,  182 


288 


Index 


Karyokineses  :   18 
Kidney,  permanent :  Chick,  216- 
217,  235-236 

Labyrinths  of  ear  :  Chick,  185 
Lacrymal  gland  and  duct:  Chick, 

183-184 

Larynx  :  Frog,  50 
Lateral  plate  :  Chick,  134 
Lens  capsule  :  Chick,  178 
Lens  vesicle  :  Frog,  43  ;  Chick, 

176 
Ligamenta   suspensoria :   Chick, 

230 
Limbs :    Frog,    4  ;    Chick,    224, 

264 

rotation  of  :  Chick,  264 
Liver :  Frog,    48 ;    Chick,    209- 

211 

blood  supply  of  :   Chick,  253- 

254 

Lower  layer  cells  :  Chick,  105 
Lungs :  Frog,  49  ;  Chick,    207- 

209 

Male  pronucleus  :   16 
Malpighian   bodies :    Frog,    83  ; 

Chick,  217 

Mandible  :  Chick,  195 
Mandibular     arch:    Frog,     51; 

Chick,  191 
Manus :  Chick,  264 
Maturation  of  egg  :  Frog,  10-16; 

Chick,  94-95 

Maturation,  theories  of:    11-16 
Maxillary  process  :  Chick,  195 
Meatus    venosus  :    Chick,    199, 

251-252 

Medulla  :  Frog,  37  ;  Chick,   224 
Medullary    canal  :      Frog,      34; 

Chick,  130 

folds  :  Frog,  32  ;  Chick,  129 
groove  :  Frog,  32  ;  Chick,  129 
plate  :  Frog,  32  ;  Chick,  129 
Membrane  bones  :  Chick,  267 
Membranous  vertebral  column  : 

Chick,  227 


Meroblastic   cleavage  :  (see  Par- 
tial cleavage) 

Mesenteron  :  Frog,  25,  45 
Mesentery :  Chick,  204 
Mesoblast  or  mesoderm  :  Frog, 

28-29  ;  Chick,  122 
changes  in  :  Chick,  212-216 
cleavage  of  :  Frog,  30  ;  Chick, 

132 
organs  from  :  Frog,  31  ;  Chick, 

277 
origin  of  :  Frog,  28-29;  Chick, 

125 
Mesoblastic  somites  :  Frog,   70  ; 

Chick,  134 
number  of,  iq  relation  to  age  : 

Chick,  134-135 
Mesonephros :      (see      Wolffian 

body) 

Metanephros  :  (see  Kidney,  per- 
manent) 
Mid-brain :    Frog,     37 ;    Chick, 

141 

Mid-gut :  Chick,  203 
Mullerian    duct :    Frog,  83-85  ; 

Chick,  233-234 
fate  of  :  Frog,  85  ;  Chick,  237 
Muscle  plate  :  Chick,  214 
Muscular    system,    development 

of  :  Frog,  69-72 
Myocoel :  Chick,  214 
Myotomes :  (see  Mesoblastic 

somites) 

Nails  :  Chick,  282 
Nares  :   Frog,  45  ;  Chick,   187 
Nasal  pits  :  Frog,  44  ;  Chick,  187 
Nephrostomes :       Frog,       78; 

Chick,  218 
Nervous  system,  development  of: 

Frog,  31-40 
Neural  arch,  canal,  fold,  groove, 

and  plate  :  (see  Medullary) 
Neurenteric  canal  :    P>og,     34  ; 

Chick,  135-136,  206 
Nictitating    membrane :    Chick, 

183 


Index 


289 


Ninth    day,     development     of : 

Chick,  281 
Nose,    development    of :    Frog, 

44-45  ;  Chick,  187-188 
Notochord  :  Frog,  27-28  ;  Chick, 

126,  155 

disappearance  of  :  Chick,  230 
vacuolation    of :    Chick,    231- 

233 

Nucleus  :  (see  Germinal  vesicle) 
Nucleus  of  Pander  :  Chick,  104 

Odontoid  process  :  Chick,  230 
CEsophagus  :    Frog,   50  ;  Chick, 

207 

closure  of  :  Chick,  205-206 
Olfactory    capsule :    Frog,    77  ; 

Chick,  267 

lobe  :  Frog,  40  ;  Chick,  173 
pit:  Frog,  44;  Chick,  187 
Opercular  fold  :  Frog,  55 
Optic  capsule  :  Frog,  77 
cup  :  Frog,  42  ;  Chick,  178 
lobe  :  Frog,  37 
nerve  :  Chick,  181 
stalk  :  Chick,  176 
thalami :  Frog,  37 
vesicle  :  Frog,  42  ;  Chick,  141, 

155,  176 
Orientation   of  embryo :    Frog, 

18  ;  Chick,  123 
Ossification  of  vertebral  column: 

Chick,  230 

Otic  vesicle :  (see  Auditory  ves- 
icle) 
Ovary  :    Frog,    87-88 ;     Chick, 

240 

Oviduct :  Frog,  85  ;  Chick,  237 
Ovum  :  (see  Egg) 

Pancreas  :  Frog,  48  ;  Chick,  211 
Parachordal    rods :     Frog,    75  ; 

Chick,  266 

Parasphenoid  :  Frog,  75 
Parietals :  Frog,  77 
Parovarium  :  Chick,  236 
Parthenogenesis  :  15 


Partial  cleavage  or  segmentation: 

97 

Pecten :  Chick,  182 
Pericardial  cavity  :  Frog,  60,  72  ; 

Chick,  270-273 
Peripheral    nerves :    Frog,    40 ; 

Chick,  173 
Permanent     segmentation :    (see 

Secondary  segmentation) 
Pes  :  Chick,  265 
Pharynx  :  Frog,  46  ;  Chick,  204 
Pineal  body  :  Frog,  39 
Pituitary  body  :  Frog,  37-38 
Placenta :  93,  172 
Plakodes :  276 

Pleural  cavity  :  Chick,  270-273 
Polar  bodies  :   II 
Polyspermy  :   17 
Primary    segmentation :    Chick, 

229 

Primitive  germ    cell  (see  Gono- 
blast)  groove:  Frog,  30;  Chick, 

124 

ova  :  Chick,  240 
streak  :  Frog,  30  ;  Chick,  123 
streak,  cross  section  of  :  Chick, 

124 
streak  and  groove,  meaning  of: 

Chick,  125 

Pro-amnion  :  Chick,  160 
Proctodaeum :       Frog,      45-47 ; 

Chick,  206-207 
Pronephros :  (see  Head-kidney) 

fate  of  :  (see  Head-kidney) 
Pro-otic  :  Frog,  77 
Proto-vertebra  :  (see  Mesoblastic 

somite) 

Pulmo-cutaneous  arch  :  Frog,  67 
Pulmonary  trunk  :  Chick,  244 
Pupil:  Chick,  182 
Pygostyle  :  Chick,  230 

Rana  temporaria  :  Frog,  I 
Reduction  division  :  12 
Reproductive  organs  :  Frog,  87- 

89;  Chick,  237-241 
Retina  :  Chick,  179 
Ribs:  Chick,  265 


290 


Index 


Scales  :  Chick,  282 
Sclerotic  coat  :  Chick,  181 
Second    day,    development    of  : 

Chick,  139 
Secondary  segmentation  :  Chick, 

229 
Segmental     duct :     (see     Archi- 

nephric  duct) 
Segmental     plate :     Frog,     70 ; 

Chick  (see  Vertebral  plate) 
Segmentation  cavity  :  Frog,  20- 

21  ;  Chick  105 
complete :  96—97 
of  the  egg:  Frog,  17-21; 

Chick,  96-103 
nucleus  :  Frog,  16 
relation  of,  to  amount  of  yolk  : 

98-103 

Sense  capsules  :  Frog,  77 
Sense     organs :     Frog,     40-45  ; 

Chick,  175-188 
Serous  membrane  :  Chick,  1 1 1 
Seventh    day,    development  of  : 

Chick,  279-281 
Sexual  eminence  :  Chick,  239 
Shell :  Chick,  90 
Shell  membrane  :  Chick,  90 
Sinus  rhomboidalis  :  Chick,  141 
Sinus  terminalis  :  Chick,  147 
Sinus  venosus  :  Frog,  60  ;  Chick, 

199 
Sixth    day,      development     of : 

Chick,  279-281 
Skeleton,  development  of  :  Frog, 

72-77  ;      Chick,      226-230, 

264-265 

Skull  :  Frog,  74  ;  Chick,  265-268 
Somatic  stalk  :  Chick,  116,  165 
Somatopleure  :  Frog,  29  ;  Chick, 

132 

Spawning :  Frog,  2 
Spermatogenesis :    (see    Sperma- 
tozoa 
Spermatozoa :       Frog,       87-88 ; 

Chick,  241 

Sperm  duct :  (see  Vas  deferens) 
Sphenethmoid  :  Frog,  77 
Spinal  nerve  roots:  Frog,  40 


Splanchnic  stalk:  Chick,  165 
Splanchnopleure :       Frog,      29 ; 

Chick,  132 
Spleen  :  Frog,  69 
Sternum  :  Chick,  265 
Stomach  :  Chick,  206 
Stomodgeum  :  Frog,  45-46 

perforation  of  :  Chick,  226 
Subgerminal  cavity  :  Chick,  105 
Summary  of  development :  Frog, 

2-4;  Chick,  114-119 
of  first  day  :  Chick,  136-137 
of  first   half   of  second   day  : 

Chick,  151-154 
of  second  half  of  second  day  : 

Chick,  162 

of  third  day  :  Chick,  220-221 
of  fourth  day  :  Chick,  262 
of  fifth  day  :  Chick,  278 
Superficial  cleavage  :  97 
Sylvian  aqueduct  or  iter  :  Frog, 

37 
Sympathetic  nerves  :  Chick,  173- 

174 

Systemic  arch  :  Frog,  67  ;  Chick, 

245 
Systemic  trunk  :  Chick,  245 

Tenth    day,    development     of  : 

Chick,'  281 

Testis  :  Frog,  87-88 ;  Chick,  240 
Thelamencephalon  :    Frog,    37  ; 

Chick,  224 
Third    day,     development     of  : 

Chick,  163-221 
Third  ventricle  :  Frog,  37 
Thyroid  body  :  Frog,  50  ;  Chick, 

211 

Tongue  :  Chick,  281 
Trabeculae    cranii :      Frog,    75  ; 

Chick,  267 
Trachea :  Frog,  207 
Transverse  process  :  Frog,  74 
True  amnion  :  Chick,  168 
Truncus  arteriosus  :  Frog,  61 
Tympanic    cavity  :    Frog,     53  ; 

Chick,  193 
Tympanic  membrane :  Chick,  193 


Index 


291 


Unequal  segmentation  :  97 
Ureter  :  Frog,  85  ;  Chick,  235 
Uro-genital  organs,  development 

of  :  Frog,  78-89 
Urostyle  :  Frog,  73 

Vasa  efferentia  :  Frog,  87 
Vascular  area :  Chick,  147,  163- 

165 
Vascular    system  :  Chick,     145, 

156-159,  198-203,  242-261 
Vas  deferens  :  Chick,  236 
Veins,  afferent  hepatic  :    Chick, 

251 

cardinal  :  Chick,  200 
cardinal,  fate  of  :  Chick,  250 
Cuvierian  :  Chick,  201 
efferent  hepatic  :  Chick,  251 
hepatic  :  Chick,  255 
hepatic-portal  :  Chick,  254 
jugular  :  Chick,  250 
mesenteric  :  Chick,  253 
pectoral  :   Chick,  250 
portal  :  (see  Hepatic-portal) 
pulmonary :  Frog,  61  ;  Chick, 

260-261 

vertebral  :  Chick,  250 
vitelline  :  Chick,  144,  199 
Vena  cava,    anterior     (superior), 
posterior  (inferior)  :  Chick, 
250-254 
Venous  system,  development  of  : 

Chick,  249-261 

Ventricle  :    Frog,     61  ;     Chick, 
156 


Ventricular  septum  :  Chick,  244 
Vertebrae  :    Frog,    73  ;     Chick, 

229 
Vertebral  column  :  Frog,  72-74; 

Chick,  226-233 
Vertebral  plate  :  Chick,  134 
Vesicula  seminalis  :   Frog,  85 
Visceral     arches,    skeleton     of  : 

Chick,  268 
clefts  and  folds  :  Frog,  51-53; 

Chick,  188-198 
clefts     and     folds,     fate     of  : 

Chick,  192-198 
clefts  and  folds,  meaning  of  : 

Chick,  192 
skeleton  :  Frog,  77 
Vitelline    membrane  :    Frog,   5  ; 

Chick,  91 
Vitreous  humor  :  Chick,  181 

Wings  :  Chick,  244 

Wolffian  body  :  Frog,  78,  82-83; 

Chick,  159,  216-220,  233 
body,  fate  of  :  Chick,  236 
duct  :    Frog,    83-85  ;    Chick, 

I5i,  159 
duct,  fate  of:  Frog,  84;  Chick, 

236 
ridge  :  Chick,  223,  237 

Yolk :  Chick,  90-92 

in  relation  to  cleavage  :  98-103 

plug  :  Frog,  23 

sac  :  Chick,  116,  165 

stalk  :  (see  Somatic  stalk) 


WORKS  BY  PROF.  A.  M.  MARSHALL 


VERTEBRATE    EMBRYOLOGY 

By  A.  MILNES  MARSHALL,  M.D.,  Professor  of  Zool- 
ogy in  Owens  College,  England.  Fully  illus- 
trated. 8vo,  pp.  xxiv.  +  640  .  .  $6  oo 

"It  is  certainly  the  best  text-book  for  student's  use  and  dealing 
with  vertebrate  embryology  known  to  me  in  any  language  ;  it  is 
adapted  in  the  most  satisfactory  manner  to  guide  practical  laboratory 
work.  I  admire  both  the  clearness  and  accuracy  of  the  author's 
descriptions." — CHARLES  S.  MINOT,  Professor  of  Histology  and 
Human  Embryology,  Harvard  University. 

"  This  is  a  great  work.  It  is  a  comprehensive  grouping  of  all  that 
is  known  and  thought  by  specialists  upon  this  most  vital  of  physio- 
logical subjects.  If  one  has  never  attempted  to  find  a  clear,  con- 
nected, complete,  straightforward  account  of  the  development  of  any 
animal,  he  has  no  idea  how  practically  impossible  it  has  been  until 
now  to  find  anything  of  the  kind." — Boston  Journal  of  Education. 

"It  is  an  admirable  book.  It  M'ill  prove  a  convenient  reference 
book  for  investigators  and  teachers,  and  an  extremely  valuable  guide 
to  students.  It  worthily  fills  a  place  heretofore  unoccupied.  I  have 
already  brought  the  book  to  the  attention  of  several  specialists  in 
embryology,  and  it  will  be  a  pleasure  to  continue  to  do  so." — 
FREDERICK  S.  LEE,  M.D.,  Demonstrator  of  Physiology,  Columbia 
College. 

"  The  book  should  be  studied  by  all  who  wish  to  obtain  as  clear  an 
insight  as  possible  into  the  present  state  of  our  knowledge  of 
embryology." — N.  Y.  Medical  Journal. 

A  JUNIOR  COURSE  IN  PRACTICAL 
ZOOLOGY 

By  A.  MILNES  MARSHALL,  M.D.,  Professor  of  Zool- 
ogy in  Owens  College,  England,  and  C.  H. 
HURST,  Demonstrator  of  Zoology  in  Owens 
College,  England.  With  48  woodcuts.  8vo, 

$3  50 

"  Has  special  value  for  students  of  anatomy." — Prof.  HENRY  F. 
OSBORN,  Princeton  College. 

G.  P.  PUTNAM'S  SONS 

NEW   YORK  LONDON 

gj  WEST  TWENTY-THIRD   STREET  24    BEDFORD    STREET,    STRAND 


THE  SCIENCE  SERIES. 


EDITED  BY  J.  McKEEN  CATTELL,  M.A.,  PH.D.,  AND  F.  E.  BEDDARD, 
M.A.,  F.R.S. 


I.— The  Study  of  Man.  By  Professor  A.  C.  H ADDON,  M.A.,  D.Sc., 
M.R.I.A.  Fully  illustrated.  8°,  $2.00. 

2. — The  Groundwork  of  Science.  A  Study  of  Epistemology.  By 
ST.  GEORGE  MIVART,  F.R.S.  $1.75. 

3. — Rivers  of  North  America.  A  Reading  Lesson  for  Students  of  Geog- 
raphy and  Geology.  By  ISRAEL  C.  RUSSELL,  Professor  of  Geology, 
University  of  Michigan,  author  of  "  Lakes  of  North  America,"  "  Gla- 
ciers of  North  America,"  "Volcanoes  of  North  America,"  etc.  Fully 
illustrated.  8°,  $2.00. 

4. — Earth  Sculpture ;  or,  The  Origin  of  Land-Forms.  By  JAMES 
GEIKIE,  LL.D.,  D.C.L.,  F.R.S.,  etc.,  Murchison  Professor  of  Geology 
and  Mineralogy  in  the  University  of  Edinburgh ;  author  of  ' '  The 
Great  Ice  Age,"  etc.  Fully  illustrated.  8°,  $2.00. 

5. — Volcanoes.  By  T.  G.  BONNEY,  F.R.S.,  University  College,  London. 
Fully  illustrated.  8°,  $2.00. 

6. — Bacteria :  Especially  as  they  are  related  to  the  economy  of  nature,  to 
industrial  processes,  and  to  the  public  health.  By  GEORGE  NEWMAN, 
M.D.,  F.R.S.  (Edin.),  D.P'.H.  (Camb.),  etc.,  Demonstrator  of  Bac- 
teriology in  King's  College,  London.  With  24  micro-photographs  of 
actual  organisms  and  over  70  other  illustrations.  8°,  $2.00. 

7.— A  Book  of  Whales.  By  F.  E.  BEDDARD,  M.A.,  F.R.S.  Illustrated. 
8°,  $2.00. 

8. — Comparative  Physiology  of  the  Brain  and  Comparative  Psy- 
chology. With  special  reference  to  the  Invertebrates.  By  JACQUES 
LOEB,  M.D.,  Professor  of  Physiology  in  the  University  of  Chicago. 
Illustrated.  8°,  $1.75. 

9.— The  Stars.  A  Study  of  the  Universe.  By  SIMON  NEWCOMB,  Retired 
Professor  U.  S.  Navy.  Fully  illustrated.  8°,  net  $2.00.  (By  mail, 
$2.20). 

10.— The  Basis  of  Social  Relations.  A  Study  in  Ethnic  Psychology. 
By  DANIEL  G.  BRINTON,  A.M.,  M.D.,  LL.D.,  Sc.D.,  Late  Professor 
of  American  Archaeology  and  Linguistics  in  the  University  of  Pennsyl- 
vania ;  author  of  *'  History  of  Primitive  Religions,"  "  Races  and  Peo- 
ples," "  The  American  Race,"  etc.  Edited  by  LIVINGSTON  FARRAND, 
Columbia  University.  8°,  net  $1.50.  (By  mail,  $1.65). 

ir. — Experiments  on  Animals.  By  STEPHEN  PAGET.  With  an  Intro- 
duction  by  Lord  Lister.  Illustrated.  8°,  net,  $2.00.  (By  mail,  $2.20.) 

12. — Infection  and  Immunity.  With  Special  Reference  to  the  Prevention 
of  Infectious  Diseases.  By  GF.ORGK  M.  STERNBERG,  M.D.,  LL.D., 
Surgeon-General  U.  S.  Army  (Retired).  Illustrated.  8°,  net,  $2.00. 

13. — Fatigue.  By  A.  Mosso,  Professor  of  Physiology  in  the  University 
of  Turin.  Translated  by  MARGARET  DRUMMOND,  M.A.,  and  W.  B. 
DRUMMOND,  M.B.,  C.M.,  F.R.C.P.E.,  extra  Physician,  Royal  Hospital 
for  Sick  Children,  Edinburgh  ;  Author  of  "  The  Child,  His  Nature 
and  Nurture."  Illustrated.  12°,  net,  $1.50. 

For  volumes  in  preparation  see  separate  circular. 

G.  P.  PUTNAM'S  SONS,  NEW  YORK  AND  LONDON. 


14  DAY  USE 

RETURN  TO  DESK  FROM  WHICH  BORROWED 

,o       ti  17    01 


This  book  is  due  on  the  last  date  stamped  below,  or 

on  the  date  to  which  renewed. 
Renewed  books  are  subject  to  immediate  recall. 


NOV  2  3  1956 


-H- 


5  )968 


NOV  2  8  1956 


OCT  2  4  196  8 


'  : 


OCT  1  0  1968    8 


"v'2.-;dJG 


N<  '121968 


OCT     91958 
SEP2DUF 


OCT  2  9  1968  J  9 


KC. 


i  9  '72 


DEC  8     1959 


'Oe5'59JM 


OCT  15  1963 


DUE 


QCT3  fl  IQRd        Subject  to  Recall 

v »  I    %j    \j    UU"  ImmAriuitttlM 


Berkeley 


U.C.  BERKELEY  LIBRARIES 

C02bl57fl75 


